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(,\:i/ittith l~l Volume 35

Volume 35

BANFlfLD & K.Il. NBAL80N

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UUN u~'f3'94SlJHijS"b

Series Editor: Paii

I H. Rlbbe
MINERALOGICAL SOCIETY OF AMERICA

GeoScienceWorld Pay-Pei~- View

Volume 35

Geomicrobiology:
Interactions between Micrcrobes and Minerals
lilian F. Banfield and Kenneth H. Nealson, editors
(this page revised 08/181201 I)

Table of Contents
i-xvi + 448 pages. ISBN 0-939950-45-6; ISBN13 978-0-939950-45-4.

Description
Microorganisms cause mineral precipitation and dissolution and control the distribution of
elements in diverse environments at and below the surface of the Earth. Conversely,
mineralogical and geochemical factors exert important controls on microbial evolution and
the structure of microbial communities. This was the rationale for the Short Course on
Geomicrobiology presented by the Mineralogical Society of America on October 18 and 19,
1997, at the Alta Peruvian Lodge in Alta, Utah.

Minerals have been known and honored since humans realized their essential contributions
to the "terra firma" and stone tools thrust our species on the path of cultural evolution.

Microbes are the oldest living creatures, probably inhabiting at least a few salubrious
environments on the earth as early as 3.8 bilion years ago. At this moment in history we are
only beginning to appreciate the intimate juxtaposition and interdependence of minerals and
microbes. We have been nudged into this position by the realization that our earth is finite,
and the recognition of many global environmental problems that minerals and microbes
contribute to, both positively and negatively. In addition, our globe may not be the only site
in the solar system where 'life' arose, or may persist.

What all of these concerns enunciate is that we as scientists only dimly comprehend our
own dynamic "terrestrial halls." This short course and volume have been generated with
great enthusiasm for grasping as much as possible of the whole panorama of possibilities
that involve both the inorganic and biologic realms.

Over 3600 mineral species have been defined and their relationships to each other and the
environments in which they form have been documented. This vast data base, collected over
the past several hundred years and constantly added to and upgraded, is a monument to the
research efforts of many geoscientists focused on the inorganic realm. Much of this data has
come from investigators intrigued by the novelty, beauty, and versatility of minerals, direct
expressions of the chemistry and physics of geologic processes. Weare now adding a new
dimension to questions of mineral formation, dissolution, and distribution: what were, are,
and wil be the contributions of microbes to these basic components of the environment.
Microbes have also been known for hundreds of years. However, their small size (0.5 to 5
Jlm in diameter) and the difficulties associated with identifying a species unless it was
grown in the laboratory (cultured), precluded thorough analysis. The advent of molecular
biology has only recently made it possible to evaluate microbial evolutionary relatedness
(phylogeny) and physiological diversity. These techniques are now being applied to study of
microbial populations in natural environments.

It is becoming very clear that the surface of Earth is populated by far more species of
microbes than there are types of minerals. Weare now exploring every portion of the globe
and finding the relationships under the rubric "geomicrobiology." The ocean deeps are
characterized by a diversity of microorganisms, including those associated with manganese
nodules. The profusion and concentration of minerals created at ocean ridges and vents
matches the variety of microorganisms, large animals, and plants there. The snowy tops of
mountain ranges and glaciers of Antarctica harbor not just ice but whole bacterial
communities whose cellular types and activities need elucidation. The equatorial jungles and
the deserts, with their enormous diversity of ecological niches, further challenge us.
The diversity of geographic, geologic, and biologic environments, including some

contributed by humans (e.g. mines, air-conditioning equipment), can now also be explored
in detail. Modern studies use protocols developed to preserve or measure in situ chemical
and physical characteristics. Electron microscopes allow direct characterization of mineral

and biological morphology and internal structures. Spectroscopic techniques permit

complimentary chemical analysis, including determination of oxidation states, with very
high spatial resolution. Other studies quantitatively measure isotopic abudances. These data
serve to distinguish biologically mediated, or biologically controlled formation of the

mineral from an abiotic process and mechanism.

Each ecological niche requires accurate characterization of the mineralogic and biologic
entities in order for us to begin to understand the range of dynamic relationships. We can
pose many questions. Is the mineral only a substrate, or is its occurrence and stability

impacted by microbiologic activity and metabolic requirements? Which minerals are of

microbiological rather than inorganic origin and what are the mechanisms by which
organisms dictate the morphology and structure of the solid phase formed? How do organic

metabolic products bind metals and change their form and distribution, with implications for
metal toxicity and geochemical cycles? How do inorganic reactions such as mineral
dissolution and precipitation impact microbial populations through control of their physical
and chemical environments? Clearly, new and excitingly research areas exist for all varieties
of scientists. Although published by the Mineralogical Society of America, the authors of

this volume include microbiologists, molecular biologists, biochemists, biophysicists,

bioengineers as well as biomineralogists. Here, they bring together their respective expertise
and perspectives to provide disciplinary and interdisciplinary background needed to define
and further explore the topic of geomicrobiology.
The volume is organized so as to first introduce the nature, diversity, and metabolic impact

of microorganisms and the types of solid phases they interact with. This is followed by a

discussion of processes that occur at cell surfaces, interfaces between microbes and
minerals, and within cells, and the resulting mineral precipitation, dissolution, and changes
in aqueous geochemistry. The volume concludes with a discussion of the carbon cycle over
geologic time. In detail:

Nealson and Stahl acquaint us with the basic properties of prokaryotes, including their size
and structure. They define the types and ranges of microorganisms and their metabolisms

and describe their impacts on some important biogeochemical cycles.

Barns and Nierzwicki-Bauer document the phylogenetic relationships and evolution of

microorganisms, begging some fundamental questions that might be now just beyond our
grasp: What was the 'last common ancestor'? The physiology, biochemistry and ecology of
hyperthermophilic, and the many diverse geologically important microbial species from the
lithosphere and hydrosphere, as well as some of the techniques employed, are presented.
Banfield and Hamers describe and integrate the processes acting on minerals and at surfaces
relevant to microorganisms, examining the factors that control mineralogy, mineral forms,
and the stability of phases. Surface properties and reaction rates for dissolution,

precipitation, and growth of impOliant classes of minerals are discussed. The possible role
of mineral surfaces in formation of prebiotic molecules needed to explain the origin of life is

examined. Litte, Wagner and Lewandowski describe biofilms, an essential interface

between microbes and minerals. They demonstrate that these membranes, with their unique
morphological and structural attributes, are sites where much activity related to dissolution
and/or formation of minerals takes place. Biology makes it possible to move molecules and
elements against a gradient. Many questions regarding the transfer of elements from
minerals to microbes at this important heterogeneous interface remain.

Fortin, Ferris and Beveridge review surface-mediated mineral development by bacteria.

Fresh or oceanic waters, anaerobic or aerobic environments provide discretely different

ecologies, bacterial entities, and resulting mineralogies. It is obvious from this presentation
that investigators have just scratched the surface of microbial mineralization processes.

Bazlinski and Moskowitz review the magnetic biominerals and provide insights into the

environmental and biological significance of these few tens of nanometer-sized mineral

products. The magnetosome chemistry and biochemistry is probably the best understood of
any biologically precipitated mineraL. Their formation and unique properties underscore the
roles these biomaterials play in the rock magnetic record and in geochemical cycles.

Tebo, Ghiorse, van Waasbergen, Siering and Caspi contribute data on the roles of
Mnminerals and Mn(II) oxidation in geologic environments. Their chapter encompasses
molecular genetic and biochemical investigations. Manganese oxides and oxyhydroxides are
notoriously difficult to identify and the crystal chemistry of these phases is a research effort
on its own. The prospect of learning how microbes utilize the multiple oxidation states of
Mn (2+, 3+ and 4+) as a source of energy sharpens the motivation for interdisciplinary

study. Manganese is also known as a cofactor in the production and activation of the
enzymes that digest large biomolecules that must be the source of the smaller molecular

species and ultimately the building blocks of C, N, 0, H required by all species. How have
the mechanisms identified in the bacterial systems been transferred up the phylogenetic tree
to plants and humans? This is an expanding and intriguing area for further investigation.

DeVrind-de long and de Vrind address silicate and carbonate deposition by algae
(eukaryotic photosynthetic microorganisms). This chapter documents the mechanisms of

biomineralization of diatoms and coccoliths. These abundant aquatic organisms are

responsible for huge volumes of siliceous sediments and calcium carbonate deposits world
wide. The implications of algal biomineralization for climatic variation throughout much of
the Earth's history may be quite significant.
Stone leads us though a quantitative approach to evaluating reactions between organic

molecules and cations. He considers available extracellular organic ligands and the roles
these play in uptake of metals. He documents the basic chemical speciation and
complexation for several elements, making metal to metal comparisons. Remaining

challenges involve coordinating the organic and inorganic results of biologic activity.

Following the discussion of biomineralization and interactions between organic compounds

and cations, Silver discusses the strategies microorganisms have evolved to deal with toxic
metal concentrations in solution. Beyond the fundamental biological significance, this has
important implications for understanding microbial populations in contaminated

environments. The impact on the geochemical form (speciation) and distribution of elements
is also discussed.

Nordstrom and Southam summarize sulfide mineral oxidation and dissolution kinetics and
devote considerable effort to describing the specific contributions of microorganisms,

mostly bacteria. Despite the vast amount of accumulated information, many unanswered
questions remain.
Barker, Welch and Banfield address weathering of silicate minerals. This topic encompasses
not only mineralogy but geomorphology, microbiology, and geochemistry. The necessary

interdisciplinary mode of these investigations is highlighted by discussion of the role(s) of

bacterial nutrition, groundwater chemistry, and biochemistry. There are obvious
implications for hazardous waste storage, a currently daunting and politicized topic that
requires predictions over thousands to milions of years.
Finally, Des Marais treats the long term evolution of the carbon cycle, adopting a

biogeochemical view. He discusses the sources, sinks and the transfer of the element over

geologic time. Consideration of such a basic series of questions relating to the partitioning

of carbon necessitate interdisciplinary crossovers. It is a fitting conclusion to a dialogue in

progress.
H. Catherine W. Skinner, New Haven, Connecticut, USA

Contents of Volume 35
Title Page
p. i

Copyright
p. ii
List of Reviews volumes
p. iii - iv

Foreward
p. v - vi
Table of Contents
p. vii - xvi
Preface
H.C.W. Skinner, p. 1 - 4

Chapter 1. Microorganisms and Biogeochemical Cycles: What Can We Learnfrom Layered

Microbial Communities

by Kenneth H. Nealson and David A. Stahl, p. 5 - 34

Chapter 2. Microbial Diversity in Modern Subsurface, Ocean, Surface Environments

by Susan M. Barns and Sandra Nierzwicki-Bauer, p. 35 - 80
Chapter 3. Processes at Minerals and Surfaces with Relevance to Microorganisms and
Prebiotic Synthesis
by lilian F. Banfield and Robert l. Hamers, p. 81 - 122

Chapter 4. Spatial Relationships between Bacteria and Mineral Surfaces

by Brenda 1. Little, Patrica A. Wagner, and Zbigniew Lewandowski, p. 123 - 160
Chapter 5. Surface-mediated Mineral Development by Bacteria
by D. Fortin, F.G. Ferris, and T.J. Beveridge, p. 161 - 180
Chapter 6. Microbial Biomineralization of Magnetic Iron Minerals: Microbiology,

Magnetism and Environmental Significance

by Dennis A. Bazylinksi and Bruce M. Moskowitz, p. 181 - 224

Chapter 7. Bacterially-Mediated Mineral Formation: Insights into Manganese(II) Oxidation

from Molecular Genetic and Biochemical Studies
by Bradley M. Tebo, Willam C. Ghiorse, Lorraine G. van Waasbergen, Patricia L. Siering,

and Ron Caspi, p. 225 - 266

Chapter 8. Algal Deposition of Carbonates and Silicates

by Elisabeth W. de Vrind-de Jong and Johannes P. M. de Vrind, p. 267 - 308

Chapter 9. Reactions of Extracellular Organic Ligands with Dissolved Metal Ions and
Mineral Surfaces

by Alan T. Stone, p. 309 - 344

Chapter 10. The Bacterial View of the Periodic Table: Specifc Functions for All Elements
by Simon Silver, p. 345 - 360

Chapter 11. Geomicrobiology of Sulfde Mineral Oxidation

by D. Kirk Nordstrom and Gordon Southam, p. 361 - 390

Chapter 12. Biogeochemical Weathering of Silcate Minerals

by Wiliam W. Barker, Susan A. Welch, and Jilian F. Banfield, p. 391 - 428
Chapter 13. Long-term Evolution of

the Biogeochemical Carbon Cycle

by David J. Des Marais, p. 429 - 448

Copyright @ 1997 - 2012

All rights reserved

360

GEOMICROBIOWGY

Quinn JP. McMullan G (1995) Carbon-arsenic bond cleavage by a newly isolated

strain ASV2. Microbiology 141:721-727
Rawlings DE. Silver S (1995) Mining with rrcrobes. Biorrechnology 13;773-778

Rochelle PA. Wetherbe MK, Olson BH (1991) Distribution of DNA

broad-spectrm mercury reistace. Appl Environ Microbiol
Rosenstein R, Nikoleit K. Gtz F (1994) Binding of ArsR, the repressor of the Siaphyi,
(pSX27) arenic resistance operon to a seuence with dyad symmetr within the ars
Gen Genet 242:566-572
Rosenstein R. Peschel A, Wieland B, Gtz F (1992) Expression and regulation of the anti
and arsenate resistance operon of Staphylococcus xylosus plasrrd pSX267. J Bacteriol
Rouch DA, Brown NL (1997) Copper-inducible transcriptional regulation from two
Escherichia coli copper resistance determinantpco. Microbiology 143:1191-1202
Schiering N, Kabsch W, Moore MJ, Distefano MD, Walsh CT, Pai EF (1991) S
detoxification catalyst mercuric ion reductae from Bacillus sp. strain RC607. Nature35

SchotteI I. Manda A, Clark D, Silver S, Hedges RW (1974) Volatilsation ofmerc\

mercurals determined by inducible R-factor systems in enteric bacteria. Nature 251:335
Salmonella typhimurium: Cellular and Molecular Biology, 2nd ed. p 1091-1102

Silver S (1996a) Transport of inorganic cations. In: Neidh FC et a1. (cd) Esche
Washington. DC

Silver S (1996b) Bacterial resistances to toxic metal ions. Gene 179:9-19

the

SiIver S, Ii G (1994) Newer systems for bacterial resistlces to toxic heavy metals.
Perspect 102 (SuppI3);107-113
Silver S, Nucifora G, Phung LT (1993) Human Menkes X chromosome diseae and

cadmium resistance ATPase: a remarkable similarity in protein sequences. Molec Miro

Silver S. Phung LT (1996) Bacterial heavy metal resistance: new surprises. Ann Rev Micr.
Environ 17:235-243

Silver S, Endo G. Nakamura K (1994) Mercury in the environment and laboratory. J J

Silver S. Walderlaug M (1995) Bacterial plasrrd.mediated resistance to mercury, cadmium

Berlin

Aspects Goyer RA, Cherian MG (eds) Toxicology of Metas. Biochemical, p 435-458 S

Sofia HJ, Burland V, Daniels DL, Plunkett G m, Blattner FR (1994) Analysis of the Es.
the region from 76.0 to 81.5 minutes. Nucleic Acids Res 22:
genome. V. DNA sequence of
Solioz M, Odermatt A (1995) Copper an silver transport by CopB-ATPase in membrane
Enierococcus hirae. J BioI Chem 270:9217-9221
Solioz M, Vulpe C (1996) CPx.iype A TPases: a class of P-type A TPases that pump heavy me
Biochern Sci 21:237-241
SlImmers AO (1992) Untwist and shout: a heavy metal-responsive transeriptional regulator.
174:3097-3101

Summers AO, Silver S (1972) Mercur resistlce in a plasmid-beng strain of Esche

I Bacteriol 112; 1228- 1236

141:323-327

Takemar K-I, Mizuno M, Sato T,'Takeucli M, Kobyashi Y (1995) Complete Iluc1eotideseq

skin element excised by DNA rearangement durng sporulation in Bacillus subtils. Mi
Tisa LS, Rosen BP (1990) Molecular characterization of an anion pump; the ArsB protein is the
anchor for the ArA protein. J BioI Chem 265:190-194
Turer JS. Glands PD. Sampson ACR, Robinson NJ (1996) Zn2+_sensing by the c

metallothonein repressor SmtB: different motifs medate met-induc protein-DNA dis

64 .

Nucleic Acids Res 24;3714-3721

Turer JS, Robinson NJ (1995) Cyanobacterial metallothioneins: biochemistr and molecular
J Industr Microbio114:119-125
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Wu J., Tisa LS, Rosen BP (1992) Membrane topology of the Ar protein, the membrane sub

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Xu C, Rosen BP (1997) Dimerization is essential for DNA binding and repression

Chapter 11

GEOMICROBIOLOGY OF
SULFIDE MINERAL OXIDATION
D. Kirk Nordstrom
3215 Marine Street

u.s. Geological Survey

Boulder, Colorado 80303 U.S.A

Gordon Southam

Northern Arizona University

Department of Biological Sciences

Flagstaff Arizona 86011 U.S.A.

INTRODUCTION

eStimates on the global flux of sulfur (Berner and Berner 1996) indicate that the

lfate from pyrite weathering, contrbuting to the average river concentration of

s.about 11 % of the tota and that this amount is increaing because of increased
tivites. Of the rock-derived sulfate contributions to river sulfate, about two-thirds

om evaporite bed dissolution (mostly gypsum) and about one-third comes from
idation. The occurence of acid mine drainage, caused by pyrite oxidation, is a
pH
.ter quality problem throughout the world. Acid mine waters typically have
range of 2 to 4 and high concentrations of metas known to be toxic to aquatic
(Ash et al. 1951, Baron 1978, Kelly 1988, Marn and Mils 1976, Nordstrom
the

1985). Acid sulfate soils, most often occurrng in lagoonal and estuarine

f pyrite (Van Breemen 1976, Pons et al. 1982). Occasionally the constrction of

nts afected by tida cycles, cause agricultural problems from the periodc

or building structures involves excavation into pyritiferous rock that requires

esigned engineering features to avoid rapid deterioration from the acid waters
.pidly develop (Byerly 1996). The sae process is also very importt in the

on the microbial cataysis of sulfde mineral oxidation to incree the effciency of

gand ennchment of sulfide ore deposits (Lindgren 1928). Biohydrometallurgists

.traction (Murr et al. 1978, Lawrence et al. 1986, Barett et al. 1993). Hence, the
of

elements to the industrial extraction of metas.

robiology of sulfde mineral oxidation has important ramifications from the global

has a long history that begins with the discovery that microbes can utiliz

association of microorgansms with pynte oxidation and the formation of acid mine

c compounds as well as organic compounds such as metabolites. S.N.

e oxidation of inorganic compounds, such as iron and sulfur (Sokolova and

adsky (1888) recgniz that some microbes could denve their metaolic energy

'ko 1968). This property afords one of the major divisions among microorganisms:
trophs, e.g. Thiobacillus spp., that gain energy from the oxidation of inorganic

nds, and the heterotrophs (like ourselves) who gain energy from the oxidation of
compounds. Autotrophs obtain their carbon reuirements for growth through CO2

is used for lithoautotroph. Organisms that reive solar radiation for

Thus, Thiobacillus spp. have also ben called lithoautotrophs. Occasionally the

0275-0279/97/0035-0011$05.00

362
GEOMICROBIOWGY

their energy source and obta cellular carbon from

photoautotrophs.

Nathanon (1902) first isolated a member of the bactenal genus Thiobacillus

its abilty to oxidi sulfur. The acidophic bactenum, Thiohacillus thiooxid

isolated and identied by Wakman and Jfe (1921, 1922) from soils con
sulfur and phosphate. Rudolfs and He1bronner (1922) observed that bacteria
zinc sulde. Twenty-five year later, th acidophilic autotroph Thiobacillus fe

was isolat by Colmer and Hinke (1947), implicat in the formation

draiage, and was found to oxidize both iron and sulfur. Numerous me
Thiobacillus genus have now ben identified and the sulfu compounds they
shown in Table 1. Oter acidophilc iron- and sulfur-oxidirs that have be
implicate in the formaton of acid mie waters are also shown in Table 1.

A.cid mie waters have ben known to contan abundant microbial life; j
ar oftn the only form of lie under these conditions. Powell and Par

later Carntor and Herndon (1933) suggested that pynte oxidation and the cons!
Table 1. Members of the Bactea gener Thiobacilus (arge alphabetically by s

Leptospirilum an Sulfobacilus; the inorganc substaces they utilize (adte from

Harson 1984 and Bartt et al. 1993, except where otherwise indicate), an four additi
spp. tht ar known to be asiate wiih acid mine waters and pynte oxidation. Acidop

Nordstrom & Southam: Sulfde Mineral Oxidation

363

gina stream afected by acid mine drainage, described acid slime streamers,

age from coal deposits may be catayze by bactena. Lackey (1938) investigated

agellates, rhizopods, cilates, and green algae. In his investigation of acidified

963a) found yeasts, flagellates, and amoebas. A.cid slime streamers of the type

,ters and soils in West Virginia and Pennsylvania, Joseph (1953) observed
tive and Gram-negative bacili and cocci, actinomycetes, fungi, green algae,
In acid mine waters from a copper mine in the southwestern United States,

1977, Johnson et aL 1979) and have been describe in fuer detail by Dugan

by Lakey (1938) ar a common occurrence (Temple and Koehler 1954,

).

the most widely studied autotrophs and a key bacterium in the catalysis of pyrite

sThiobacillus ferrooxidans. It was isolated and identified as Gram-negative,

of acid mine waters (lthen et aL 1953). Following these discovenes, there

, and rod-shaped by Colmer and Hinkle (1947), Colmer et al. (1950), Temple
r (1951), and Temple and Delchamps (1953) and shown to be essential to the

onsiderable reseach on both the abiotic and the microbially-catalyze reactions

mineral oxidation. By the 1960s, the essential role of bacteria in the oxidation of
ially in coal, had been well-established (Lyalikova 1960, Silverman et aL.

S., 52032-,53062-, S4062-

H25,52032.

at sulfide surfaces ar poorly understood. In this chapter we attmpt to

complicated, rates and mechanisms are diffcult to resolve, and the interations

principal activities have motivated studies on microbial catalysis of sulfide

the need to elimnate or reduce the deleterious effects of acid mine drainage and

Thiobacilus albertis
H2S, 5., 52032-, S4062-

are shown in bold type.

T1iicbacilus acidophilus 1
5.,52032-, S4062-

f metas from ores and mine waste matrials. The reactions and the microbial

ges gained in biohydrometalurgy when bacteria ar used to improve the

Thiobacillus denitrificans
Thiobacillus delicatu

Thiobacillus tepidrius

Thobacilus novellus
Thiobacilus perometablis

Thiobacillu neapolitanus

Thiobaci/us haophilus2
Thiobacillu intermius

S., S2032-, S4062-

H2S, sulfide mineras, S.

H2S, S., S2032-, S3062-, S4062-

S2032-,84062S', S2032-, S4062-

HzS, sulfde miners, S',

H28, sulfide minerals, S.,

S'
S., S2032-, 5462-

oxygen. The overall reaction is commonly written as

ebasic ingredients responsible for the formation of acid mine waters are pynte,

the current state of knowledge of sulfide mineral oxidation with a focus on the
eria in this important process.

Thiobacilus thermphilica3

HzS, sulfide minerals, S.,

Thiobacilus ferrooxidall

Tliiobaciluii thiooxidans

HzS, S203z.

matters, other oxidizing agents have ben implicate, chiefly ferrc iron.

s with as many possible rate-determning steps to consider. To furter

at a time (Basolo and Pearon 1967). Hence, there could be 15 or more

Cannot take place in a single step. Only one or two electrons are commonly

nof oxygen. In addition, the iron is hydrolyzed and precipitated. These

trons ar lost by oxidaon of disulfide, and 15 electrns ar gained by the

mole of pyrite oxidized in Reaction (1), 1 electron is lost by oxidaton of iron,

ement content. All of these properties of pynte ca afect the rate of reaction.

crysta forms and with large varations in defect strcture, crystallinity, and

curs over a large range of grain size and surface area. It also occurs in several

ating features are tabulated in the following list:

of chemistr and the actual processes ocurrng in the environment. Some of

rite oxidized. This reaction, however, is extraordinarly simplistic compar to

2 + 15/4 O2 + 712 H20 ~ Fe(OHh + 2 H2S04

(1 )
mole of ferrc hydroxide and two moles of sulfunc acid ar produced for every

MARY OF SULFIDE MINERAL OXIDATION REACTIONS

Thiobacillu versut

Fe2+, S.

S'
S'

Fe2+, S., sulde miners

Fe2+, S., sulfide miras

Fe2+, sulfide mierals

Fe2+, sulfide mieras

Thiobacilus t1iioparus4

Leptosplrilum ferroo:ddans
Leptospiril,n thermoferrooxldans
SlIlfobacilus thermosuljulooxidans

Arhae sp.
Acidianus brierieyl
SulfGlobus solfataricus
Sulfolobus ambi"alens

Sulfolobus acidocaldarius

i Also known as T. organoparus

2 Woo and Kelly, 1991
3 Egorova and Deryugina, 1963 (not a Thiobacilus sp.)
4 Range of pH = 3 to 10

364
GEOMICROBIOWGY

Fortnatly al the intermedat retions nee not be determecl t

contrllng mechanisms involved with pyrite oxidaon.

(3) The product of pyrite oxidaton is not a pure ferrc hydroxidelih
phass with varable stoichiometr, including:

goete (a-FeOOH), ferrydrte (FesOHso4

jarosite (KFc3(S04)z(OH)6), schwertante (FegOgS04(

(4) Products, such as elementa sulfur, have ben found to form frompy
Importt reviews on pyrte oxidation have ben published by
Nordstrom (1982), and Evange10u (1995). Reviews on the oxidaton of

minera sulfdes can be found in Dutr and MacDonad (1974) an

Alpers (1997). This section highlights the major findings from thesere

current resarh.
Stokes (1901) reognized tht the oxidation of
pyrite by ferrc iron
a long time. The following balance chemical retion
FeSi + 14 Fe3+ + 8 HiO =l 15 FeZ+ + 2 SOi- + 16 H+

has ben confirmed by several experimenta studies (Garels

Wiersma and Rimstidt 1984, McKibben and Bames 1986). Since
circumneutral pH values, Reaction (2) requires acidic conditions.

oxidi more ferrc iron from ferrous:

Fez+ + 1/4 0z + H+ =l Fe3+ + l/2 HzO

Nordstrom & Southam: Sulfide Mineral Oxidation

scopy. Several studies on both ai and ai-satuated aqueous solutiol1SQl

ixidaon and acd leahing of other su1fide minerals have also ben subjec

ion have shown the formation of a Fe(i oxyhydroxide by diffusion'

the surace and oxidation (Buckley and Woods 1985, Pratt et al. 1994a;b
995). Underneath ths layer is a sulfur-enrched layer that wil eventuall)

.0

(Mycroft et al. 1995). The oxidation of chalcopyrite in ai also lea to iroI

e surac and formation of an Fe(il oxyhydroxide leaving a residual CuS.

80 to 100C, most of the sulfur from the oxidaon of chalcopyrite app:

and Woods 1984). Chalcopyrite oxidaton in acid solution lead to th;

dissolution of iron and a residual CuS2 surface (Yin et al. 1995). A

surac but arsenic also migrates to the surace and rapidly oxidis ani

ulfur (Dtrza i 990). Arenopyrte oxidation also form Fe(ll oxy

in contat with water (Nesbitt et al. 1995).

and sulfate furter complicat the chemical interpretation. One of thi

.tiori of unstable sulfoxyanons of intermedat oxidation sta betweei

was from Steger and Desjardi (1978) who found a thiosulfate compouni

of pyrite undergoing oxidaion. Recntly, a copper thiosulfate minera ha

from the oxidation of copper sulfides. Sulfoxyanion formation from pyriti
H values of 6 to 9 was studied by Goldhaber (1983) who found thiosulfate

sulfite but only at high stirring rates. The proportons of sulfoxyanion

t. the solution pH. Polythionates were dominant at low pH, thosulfat wa
and

rre iron relac oxygen as the oxidant, sulfoxyanions were no longe

rate Go1dhaber's results with improved analytical methods, but they foun!

igh pH, and some sulfte formed at the highest pH values. Moses. et al

absence of oxygen. Neverteless, the overall rate of pyrite oxidation in a

but the oxygen does not have to diffse to the pyrite surfaces. Pyte ..ca

mine, or in a waste rock pile wil largely be determned by the overa

at exactly 0.5 mole fraction of arenc substitued for sulfur.

ctual solid solution exists between pyrite and lllngite (peAs) with arenopyrite lI II stabl

Id be definitive in distinguishig these sources. Thiosulfate, sulfur, sulfite, an

ar not liely to be found from disulfde oxidation beuse the autocyt

of acidic mie tailings (Fortn et al. 1995). Stable isotope compositions c

retions for sulfide mineras. The ocurnee of hydrogen sulfide,. sulfur, an;
in mie waste environments indicate eithr sulfat reduction or acid dissolutio
lfides. Viable, dissimiatory sulfatereucing bacteria have ben found withn th

m oxidaon of HzS. Ths distiction is fudamnta to the nature of aci

orm sulfu during acid dissolution at 28C and pyrte does not. The sulfu

sul and thosulfate upon oxidave attk in acid solutions, dependig OJ

tion of oxidats, and temperatu. Ahonen et al. (1986) have shownth~

'on state of S( -1) intermediate between S( -ll and S(O) and a tendency to forn

owever, do not form HzS, upon reaction with acids. Disulfdes conta sulfu

rm sulfur, thiosulfate, sulfite, and, ultiatly but more slowly, sulfate. TIl

. The monosulfides react with acid to form H2S (Parsons and Ingraham 1970)
increing with increasing solubilty. Upon contat with air, H2S wil rapidl:

and millerite, NiS) and the disulfides (such as pyrite and marcasite, FeS2, ani
,;FeAsS ). Mieras such as molybdenite, MoSz, and chalcopyrite, CuFeS
. sUlfides beause the sulf atoms are bonded to meta atoms and not to othe

.aton of oxidaton products from sulfide mierals depends on the ty ani

of the minera. The first simple distiction is between the meta monosulfide
alerte, ZnS, greenockite, CdS, covellte, CiiS, pyrhotite (Val. troilte),

'y ferrc iron.

.ese results implicate ferrc iron as a powerfl oxidant for al types of reuce,
es..Wllamon and Rimstidt (1993) have demonstrted the rapid oxidation 0

transport (advection, convection, and difusion).

Elementa sulfur may form during pyrite oxidaton, but the mechansm
understood. At ambient envirnmenta temperatures, litte or no sulfu

formtion of sulfu during pyrite oxidaton incre with temperare.

found that detetale sulfur appe at 6OC and Lowson (i 982)
formaton rehes a mamum at 100-150C. Both authors al found that
ru times, increased ferric iron concentration, and increased oxygen coneen
the production of sul.

When pyrite is atked by acid solutions, the iron is easily leahe frm

layer, leaving a sulfu-rich surfac. Buckley and Woods (1987) reviewed

photoelectron spetroscopy (XPS) literat on the surface oxidaon. Of

discussed the effect of experimenta tehnques on the results. They also cone
their own work that iron tends to be easily leahed from the surfac produc

deficient (or sulfide-rich) surace that does not have the propertes of ele
unless prolonged strong acid atk was used. Several other studies, usi
Raan spectroscopy, have confired the intial dissolution under acidic condi
releases iron and form a layer contaning disulfide, monosulfde, and polysulfid
1994, Nesbitt and Muir 1994, Sasak et al. 1995). With continued oxidaton m
decreaes, disulfide increes proportonally, polysulfides increase, and

thiosulfate and sulfat form (Nesbitt and Muir 1994). The formation of the disulf
corrborates the early work of Sato (1960) on the mechansm of oxidation of s
boies. The degradaton of this surace by either ferrc iron or microorganisms,
a critical and porly understoo aspet of pyrite oxidaon. As Norrs (1990) and
al. (1995) mention, this sulfur-rich surface shuld be energeticay favo.

Thiobacllus thiooxidans and may explain their association with T. ferrooxidans.

366
GEOMICROBlOWGY

oxidation on a semi-conducting surface such as pyrite is much too rapid. The

Goldhaber's experiments cannot be reproduced without using very fast stirring r
high shearng force at the mineral surface. The results of thosulfate formation fro
oxidation in the column leahing experiments of Grager and Warn (1969) wen
(Nordstrom and Alpers 1997) beause they containated their columns with
sulfide solutions. Dissolved sulfide rapidly forms thiosulfate when exposed to the
Galvanic protection has been postulated to afect sulfide mineral oxidation

1964). The more electroconductive the meta sulfide, the slower its rate of ox

the weathering of mineral deposits (Sveshnikov and Dobychin 1956, Sveshnikov

whereas the less conductive sulfides exhibit increased reaction rates as long as th

Nordstrom & Southam: Sulfule Mineral Oxidation

oxidation reactions. Indirect oxidation OCCurs through microbial

errous to ferrc ion oxidation (Reaction 3) and then direct oxidation

acidocaldarius to pyrite surfaces is rapid (Bagdigian and Myersn

errc ion (Reaction 2). Adsorption of either Thiobacilus

ore 1987, 1988). Surface etch patterns that reflect bacterial attahment

TH2

516, RV78

Bn

B54, RT63, NB72, 576,

BAS7, 161, 06, 176

0C

B54,L6

Microbial reference

P91, B93

P91

B54, BIS8, SE64, 091,

Microbial

Table 2a. Oxdaon stdi on irn sulde mira.

WR84,R9

Abiotic reference

MB86, '8J89, M1l7, MH91, R94

MH1, N94, 091

B54, ross, 083, MB86, M87,

FeS;!

TC6, NS94

electronic contat with the more conductive sulfide. Kwong (1995) has demonstr.
process and has shown that relative rates can be predicte acording to the seq
standard electrode potentials as compiled by Sato (1992). Furtermore, K won
(1995) have shown that although bacterially-medat oxidation increases the
rates, the electrochemical sequence remains the same.

Fei_xS

Form
CusFes.
Co;CuS,
CuFeSi
CU2S

1167, M11, J:M74b, WR86

Table lb. Oxdation stdies of copper sulfdes and selenides.

Compilation of sulfde mineral oxidation studies

We have compiled 29 minerals for which oxidation studies have ben
temperatues below 50C either with or without microbial paricipation. This
primarly on the reviews by Dutrc and MacDonald (1974a), Ehrlich (19

Nordstrom and Alpers (1997). More information and references can be found
reviews. Th following compilation has been subdvided into four tables (Tables
which the iron sulfides ar found in Table 2a, copper sulfides and selenides in
arsenic and antimony sulfides in Table 2c, and the remaining sulfides in Table

have also been placed in alphabetical order within eah table. A few commnts
here. Of course, many more studies have been done on minerals like pyrite

referenced in this paper. The studies with valuable rate information have been p
included. The references themselves are given in shortand notation and decoded

S30b,

CuFe2SJ

T67

D70e

CuS
CUgSS

K66

of all the tables. In most of these studies the surface areas were not
Furthermore, the effect of ferrc iron concentratons were not always obt

CU2Se

K66

distinguished from microbial action. All the necessar rection products were

determned so that the stoichiometr is not always known. In that regard, E

Cll2Te

CU12As.SI3

SiSi

As

B534, Y80

S33, BS34

TT63

533, '8534, K052

R9

'854

T74, TG77

E63b

E631i

178

EM

SC61

EM

Abiotic reference Microbial reference

Table 2c Oxidation studie of arnic, antiony, and galum sulde.

CuSe

found the pH to decrease during enargite oxidation by T. ferrooxidans but it

the abiotic control. The chemical interpretation would suggest that copper w
and oxidized in both solutions but that the sulfur and arenic were oxidized
presence of bacteria.
Most of the microbial studies included a sterile control but were not nece,
the abiotic references. Qualitative to quantitative data is commonly available
microbes increase the rat of reaction when compared to the sterile control

mechanism are unclear. Many of the studies used impur minerals.

experiments were, of course, done to improve meta extrtion from

provide quantitative rate information.

Role of bacteria
Although the association of microbes with sulfde mineral oxidation has
for many decades, it has taken a considerable amount of researh to dete

mechanisms, and metabolic pathways. Discussion has focused on w

primarly the genus Thiobacilus, degrade sulfides by a direct or an indi

mechanism (Silverman 1967). During dirt oxidation, the bacteria atth

the sulfide mineral surface and directly solubilize the surface

CU12Sb.Sii

368

Mineral

ci

GEOMICROBlOWGY

Abiotic reference:
PS9. B7S

SS9

Bn,174

ST4. TS74

171, 174

Table 2d Oxidaon studies of oiler meta sude.

Fol?la
HgS

CoS

H70.R94

RT63. DT64.1l.14
DM74c

BAS7. BISS. B6S. BMj

RH2, 161. MPl. TIi,

Nordstrom & Southam: Sulfde Mineral Oxidation

369

ulfide minera oxidation studies, the microbial physiology of Thiobacilus

idans, and the microbial ecology of mine waste environments.

AQUEOUS Fe(H) OXIDATION KINETICS

aqueous oxidation of ferrous to femc ion has been firmy established for acid

where the rate is relatively slow. The rate increases with increasing pH but also
sensitive to oxygen and anionic ligand concentrations. At circuinneutral pH
eabiotic rate is so fast that bacterial catalysis has not been clealy demonstrated
ot needed to explain the rate of aqueous iron oxidation. Singer and Stumm (1968,
owed that the rate increased rapidly with increasing pH above a value of about 4.

is value the rate leveled out and beame nearly independent of pH at about 3 x

to about 3 X 10-7 mol L-1 S-1 (Singer and Stumm 1970a,b). This catalysis is

IL-1 s-1. The presence of T. ferrooxidans increased this rate by five orders of

llM7 Bii il Mun (1973)

BLn Biiy im Le !lou (197

Bl11 Bro IlJIl (1989)

:B5l Diy il lamel (195l)

BAS7 II im An (l91S)

893 B!. ei ai. (1993)

1111 S.i en!. (1989)

D7S Bi et ai. (1915)

Bn Bm(197

1m Il ei ll. (1971)

865 81i et ai. (196)

854 &y ei II (1954)

N9 Nl (199)

MH1 Moc li He (1991)

MB86 Mc II B_ (198

M7i Mul (1911)

M81 Mii ei ai (1987)

M69 Mul (196)

L10 Lo (91)

L6 La ei ai (196

KR71 KI li Ra (197

K0lCylov li Odv (196)

K06lCylov il Odv (1%3)

KG52 lC il Ory (i9S2)

K66 K!manil ei ai (196

16 Id (196)

TI12 Ton il 1(1

Tl Th il Ii

176 Toi co II. (1916)

174 Toi et ai (1914)

171 Too(1911)

'l7 Th co ai (196

ST4 Sil_ aD Too (197.

SE Silvm li Fi

SC1 Su_il

516 Sa el d. (1976)

S33 SuIvi (1933)

S31 Sulva (1931)

S:l Sulva (193)'

rat to var 2-8 X 10-7 mol L-1 s-1. He found the rae in the same drainage to

easured stream velocities in some acid mne waters in California and found the

water in Japan but the strea velocities were not directly measured. Nordstrom

itions.

. This agreement is quite good considering differences in experimenta procedure

cot sulde
PbS

CdS
US2.

NiS

MoSi

R9

(Fe, Ni~s

Zi

able in the enhancement of inorganic reactions and has a major effect on pyrite
g.Measurements from microbial oxidation experiments, to study optimal growth

BS3 Bro aD Sullvi (1934)

N1 N'ielsll Bec (191)

TS4 Taran

Table 2e. Refemnc on oxidaon stdi of sude mi

D6 Dm ei Il. (196)
D7 Dulr ei ai (1910a

NS9 N'do il Sc (199)

'l Tuiov im Tini (

17 Tor (197)

TC6Tecll~

R9 Rl et ai (199)

WR Wal il Ri (

WR Wle an

00 Uc (196

TG71 Tonll Oa (l

tu R. il Heii(92)

Yl Yii co ai (I'

Michelis-Menten equation that contains both a first order and a zero-order term.

:ro order. Bacterial cell division by binar fission, is the separation of a parent
o daughter cells. During the lag phase and exponential growth phase, the growth
.ent on ferrous concentration and a first-order or pseudo-first-order reaction rate
observed. The convention in microbiology is to trat this changing growth curve

rate can beome independent of the ferrous iron concentration and the rate

beCome high enough that the growth rate becomes constant and independent of
tion. For a lithoautotroph like T. ferrooxdans, this means the ferrous iron

build-up of toxic products, or by a metabolic inhibitor. Nutrent concentrations

that after a period of time with litte apparent growth, known as the lag phase,
apid growth that can only be stopped by lack of an energy source, an essential

doubling process, however, is exponential (like radioactive decay in

sometimes non-integral order. The rate equations for living entities such as
more complex than for the simpler entities of molecules and atoms. Growth
icrobes, expressed as population densities over time, usually follow a sigmoida
e. During the early phase of growth at low cell counts, there is litte change

kinetics, reation rates ar generally zero-order, first-order, second-

is needed here regarding the units and formalism for microbial reaction

hydrologic conditions, nutrent limitations, and UV radiation for suiface

res are about !00.

30C. In the environment, however, ferrous iron oxidation rates
be lower because of numerous environmental factors including temperature

culture media (usually 9K medium, Silverman and Lundgren 1959) and where

a rainstorm, presumably due to the flushing out and dilution of the bacterial
pH values of 2-4, the microbiaIly-catalysed oxidation of ferrous iron
an average optimal rate of 5 x 10-7 mol L-I S-1 whether in the field or in the

experiments. Wakao et aL (1977) estimated a rate of 3 x 10-6 mol L-I S-1 for an

detennnations of the ferrous oxidation rate are very similar to those derived from

and Lundgreii 1959, Lundgren et aL 1964, Lay and Lawson 1977, Noike et

mOb Du 'il!. (197)

001 Ols (1991)

'ooxidans on culture media, typically gave rates of 2.8-8.3 x 10.7 mol L-1 $-1

DC De Cuyp (196)

P39 i' (1939)

Tn Tor elli. (1m)

DM4i Du il Ma (1974b)

F91 PI (1991)

E6 Eh (196)

am R.U aD Tni (1%3)

MP1 Mall Pr (1%1)

DM74b Duir im Ma194c)

US2 Uwa (1952)

Gl3 Qi (198)

IW7S RkIlV..(I97)
S3 Sulva (1!O)

Dl64 Dm il Tr (196)
E63b Eh (1963b)

mo Ha_ eia!. (1910)

161 1"" et ai (1961)

of

observed (Bennett and Tributsch 1978). The actual mechanism of enzymatic oxid
not entirely clear and is discussed furter in the section on "Microbial Oxidation

Minerals," below. Furthermore, it seems unnecessar to explain the rat data. Wi

explore this controversy and the general interaction of bacteria with oxidizing sulf
reviewing the empircal rate data for both ferrous to ferrc oxidation and pyrite oxi

370
GEOMICROBIOLOGY

studies on the microbial rate of ferrous iron oxidation have shown the rate to be

The rates we are using assume nutrent-saturated conditions and zero-order rates.

for a wide range of ferrous concentrations (Schnaitman et al. 1969, Okereke

1991). The rate of sulfide mineral oxidation wil now be considered.

SULFIDE MINERAL OXIDATION KINETICS

The conventional approach to distinguish between the diect and indiect

mechansms would be to compare the ra of pyrite oxidation by iron-oxidii:n

with that obtaned abioticay but in the presence of ferrc ion. This analysis, ho
oxidation of pyrite by Fe(Il), (2) oxidation of Fe(I!) by bacteria, and (3) oxi

more complicated. It is known that acidophilc iron-oxidizing bacteria wil gen

from Fe(l). The question that should be addressed is: what are the relative rates
pyrite by bacteria independent of their oxidation of Fe(ll)? If there is a diret mee

significant, it would have to be as fast or faster than the rate of Fe(IT) oxidation

bacterial pyrite oxidation other than by regeneration of Fe(Il) then for that

should be a plausible mechanism to explain it. Under those circumstances, the

these concepts in hand, let's look at the evidence.

pyrite oxidation rate would have to be faster than the abiotic oxidaon rae by Fe(

Nordstrom and Alpers (1997) compiled several reports on pyrite oxidation

summar results are shown in Table 3. The oxidation rate with ferrc ion as the
faster than the rate with oxygen as the oxidant by an order of magnitude or more.
these rates overlap when comparing different investigations, the relative rates w
one investigation show a consistently faster rate with Fe(Ill). Most investigators
in

(at pH = 2, T = 2YC) close to 1 x 10-8 mol m-2 S-l which would be less than.9 x
m-2 S-l for the bacterial rate. These results would indicate an enhancement

microbial athment. Unfortunately, par of this difference could be explained b

preparation effects and experimental design problems. Furthermore, the microbial
at least 2 or 3.

obtained by assurrng a surface area based on grain size which could be low by

Abiotic Rate
3 x l()12 mol L-l sol
1 - 2 x l()s mol m-. S-l

0.3 - 3 x 10-9 mol m-' S.l

8.8 X l()8 mol

Table 3. Comparson of iron and pyrite oxidation rates,

Reaction
Oxdation of Fe(T
Oxdaton of pyrite by Oi

Oxdaon of pynie by Fe(II

Nordstrom & Southam: Sulfde Mineral Oxidation

371

n (1991) reported his results in terms of the rate of formation of aqueous iron

as 12.4 mg Fe L-l h-1 or about 6 x 10-8 mol L-l s-l. This rate is about one order of
de. Jess than the fate of bacterial oxidation of Fe(IT) suggesting an inhibiton of
idation by the bacteria. The inhibiting effect of adsorbed bacterial cells on the

rface was reported by Wakao et al. (1984) who concluded that pyrite oxidation
by the indirect mechanism through the growth of free-floating ferrous-ironbacteria. In the experiments of Wakao et al. (1984), a suractant was used to

e ceJls from the pyrite surface and the oxidation rate then increased again to near
.er leveL. Contradicting the experiments of Wako et a1. (1984), Arkestyn (1979)
e rate of pyrite oxidation to decrease when he separated T. ferrooxidans from the

urfaces by a dialysis bag. The observation that iron-oxidizing bacteria can oxidize

Fe(IT) faster than they can oxidize pyrite may indicate inhibition by bacterial
tion on surfaces or, more likely, it may indicate the rate of pyrite oxidation by Fe(il
er than the oxidation rate of Fe(l) by bacteria. This conclusion would be consistent
general observation that aqueous chemical reactions, espeially when catalyzed,
r than heterogeneous chemical reactions.

for the indict oxidation mechanism. They pointed out that subculturing T.

view by Sand et at (1995) summarzed reent literature and provided further

n. The bacterial cells could not function in the absence of iron. Furter

'ans in an iron-free salt solution resulted in complete loss of measurale substrate

ost, i.e. exopolymers, by washing. The extracellular polymeric substance

ed work of theirs showed that the iron in the bacterial cells could not be removed

empha.~ized the importance of thiosulfate as the first soluble oxidized sulfur

rs) faciltate the attachment of the bacteria to the pyrite surface. Sand et aL.

a key intermediate during the oxidation of pyrite. Thiosulfate is oxidized to

and hydrolysis of tetrathonate produces disulfane sulfonate which furter

es to form a varety of products. Furter elucidation of sulfoxyanion formation

of polythionates is to be expected since both Fe(ll) and pyrite can catayze the

leaching of pyrite was reported by Schippers et at (1996). They monitored the

of thiosulfate, elemental sulfur, polythionates and sulfate during pyrite oxidation
. ferrooxidans and L. ferrooxidans in solutions with pH just less than 2. The

ition of thiosulfat to polythionates abiotically, These two studies find no

for the direct mechanism and substantial evidence for the indirect mechanism.

is slower than the conversion of Fe(II) to Fe(il by bacteria and slower than the

onsistency and precision of the rate data indicates the abiotic pyrite oxidation rate

of pyrite with bacteria and Fe(T. However, severa caveats should be noted.
aqueous Fe(ll) oxidation rate is the maxmum possible rate achievable with no

utrents and at optimal temperatures. Microbes in the environment ar nearly

wth-limited by some necessar nutrient, predatory relationships, hydrologic

ntrolled by bacterial growth rates and these, in turn, wil be controlled by

, or by other factors. Hence, their environmental growth rate wil be slower than
quoted above and they could be less than and probably not greater than the rate
xidation by Fe(Il) Furtermore, the oxidation rate of pyrite in the environment

The sourc of the bacterialy-medated pyrite oxidation rate study (Olsonl99

interlaboratory comparson implemented with sterile controls. About a 34-fold.i
rate was observed with T. ferrooxdans present compared to the sterile contr'

e overall rate is governed by environmental factors that afect the growth rate of

of pyrite ar fast and comparable in the presence of iron- and sulfur-oxidizing

xperimenta rate studies is that both the rates of aqueous Fe(IT) oxidation and the

and nutrient limitations. The search for the rate-determining step and mechanism
aton of acid mine drainage may be over. What we have leared from all of the

nta factors such as temperatre, hydrologic varables (supply of water and

control gave similar (but higher) rates to those from other studies of pyrite ox

oxygen. Pacorek et al. (1981) sirrJarly found a 25-fold increase in the

catayze pyrite oxidation rate relative to the abiotic control. Liza and Suz'
found that the pyrite oxidation rate with T. ferrooxdans and Fe(Il) was notably

the abiotic rate with Fe(IT!). These results, however, could be an ar

experimenta design, When iron-oxidizing bacteria ar oxidizing pyrite, th
regenerating ferrc from aqueous ferrous iron whereas the sterile control has a
ferrc concentration that eventually gets used up so that the reaction rate slows .d
complication is diffcult to avoid in experimenta studies.

372

GEOMICROBIOWGY

The link between the chemistr and the biology of sulfde miera oxidatio
expressed as follows:

maximize their effciency of substrate utilzation. The close adherence redu

(1) Bacteria want to be attached, or as close as possible, to sulfde mineral

A!

needed for diffusion of iron between the minera and the bacterium,it
necessarily reuire a separate mechanism for sulfde mineral degradation.

also changes the surface chemistr of the solid-microbe inteiface (see section

(2) Al available evidence is consistent with a chemica oxidation of sulfide

aqueous catalysis by iron- and sulfur-oxidizing bacteria.
(3) No other procsses need to be invoked to explain the available data. Thiss

another expression of Occam's razor.

MICROBIAL OXIDATION OF SULFIDE MINERALS

General physiology of Thiobacilus ferrooxidans

Thiobacillus ferrooxidans is tyically known for its abilty to oxidize reuc,

compounds and ferrous iron to produce sulfuric acid and femc iron as by-prod
metabolism (Ingledw 1982, Harison 1984). The genera nutrtional requireme
bacterium are provided by carbon dioxide fixation (providing cellular carbon;
1956), pyritic minerals as sources of energy (see Table 1) for ATP, ammonia,
nitrogen, or nitrate as its source of nitrogen (Temple and Colmer 1951, Lurid
1964, Mackintosh 1978, Stevens et al. 1986), and phosphate from acid solub

available phosphate mineras (Lipman and McLe 1916). Previous report

Fig.

heterotrophic ability of T. ferrooxidans ar actually a consequence of the.p

acidophilc heterotrophs found to co-exist with T. ferrooxidans (Harson et at 1
The formaton of ATP occurs via a chemiosmostic mechanism (see

impermeable natue of the cytoplasmic membrane to protons maintans a pH(p

pH 6) based proton motive force, allowing protons to be transported only at si
ATPase is anchored in the inembrane (Ingledew et al. 1977). In addition to.'
general cell energetics, the A TP that is fonned by this reaction is used in rever
transport to produce NADPH (AJeem et al. 1963) which is in turn used inth
assimilation (fixation) of CO2 by the Calvin-Bensen cycle (Maciag and Lundgre
In natral systems that contain iron, T. ferrooxidans may exclusively oxidi
Fe3+ to gain energy. This oxidation, yields a chemically reactive cation which can

electrons from less electronegative meta species (e.g. pyrite, Eqn. 2; Mehta
1982) formng ferrous iron once again. The formation of reduced iron from
provides an effective bacterial electron carer for sustaned Iithotrophy. Mineral
then, is a chemical process enhanced by bio-catalysis (Singer and Stumm 1970,
Murr 1982, Hutchins et aL. 986, Baldi et al. 1992).

The oxidation of iron yields low levels of energy. Silverman and Lundg
calculated 18.5 moles of iron need to be oxidized to assimilate 1 mole of c
calculations assume 100% metabolic effciency which is not possible in biological

For Thiobacillus ferrooxidans, metabolic effciency has been found to be highly

(3.2%, Temple and Colmer 1951; 4.8-10.6%, Beck and Elsden 1958; 20

Silverman and Lundgren 1959; 30%, Lyalikova 1958). The poor energy yieldr'
utilization from iron oxidation remains a puzzle.

In our model (Fig. 1) of iron oxidation in T. ferrooxidans adapted from

(1977) and Blake et at (1992) the biological oxidation of Fe(II) to

Nordstrom & Southam: Sulfde Mineral Oxidation

Pyte
Fe?+

Fe'+ I

14Fe'" + Fe&. + 8H20 -; 15Fe2+ + 250/' + 16tl

F'.... Fe?'

Rusticannz,

J- 7 \ I
2Fe2+X Cyl ci

2H' + %02 + 2tf -. H20

2e'

Ruslicyann +1

0;

2Fe" Cyt C

OUTSIDE OF CELL (pH-2)

PEPTIDOGLYCAN

PERIPLASM

(pH-2)

PLASMA MEMBRANE

(pH-6-7)

CYTOPLASM

T; ferrooxid based on a bidirectional diffuion gradient for Fe(TI).

373

mode! (adapted from Ingledew et al. 1977, and Blake et al. !992) for the bioenergetics of iron

al oxidation of pyrte by Fe(UI) creates a bidiretional diffusion graient which

lydrives Fe(m into the periplasm and Fe(Im out of the periplasm. Iron wil

y (if at al) to the organic constituents on the cell surface and in the peri
plasm
.ey wil be outcompeted by protons at pH 2. Other aspets of the model ar the
ose described in the model ofBJake et al. (1992).

,indirect oxidation of non.ferrous sulfide minerals

ooXidation of sulfide mineras presents a speial problem when iron is not a

the minera1(s). In these systems, the direct, enzymatic of susceptible minera

ben proposed in which each bacterial cell acts as a conductor of electrons

of

rystal strcture of chalcocite to oxygen (Erlich 1996). The transfer of

d Ritidt (1984). Whe these models ar supported by an extrmely close

electrons from pyrite under acidic conditions has also been described by

Tributsch 1978, Norman and Snyman 1987, Southam and Beveridge 1992),

.neral interaction (Bagdigian and Myerson 1986, Duncan and Drummond 1973,

of free electrons from the crystal structure only represents a paral reaction and

374
GEOMICROBIOWGY

cannot occur without an appropriate bacterial electron acceptor. The outer memh
of Gram-negative Bacteria, e.g. T. ferrooxidans, functions as a passive diffusio

1977). Therefore, mieral sulfide oxidation must proceed via diffusion of

(Beveridge 1981, 1988) and does not possess electrn acceptors (Haddock

present in iron-containing systems (described above; Fig. 1), acid dissolution ofc

compounds across the outer membrane into the periplasm. Soluble ferrous iron

releases soluble Cu+ (Nielsen and Beck 1972) and nonbiological, autooxidation of
under acid conditions produces elemental sulfur (Rickard and Vanselow 1978) rn
from oxidation of H2S formed during acid dissolution of a monosulfde,

CuS + 112 O2 + 2 H+ ~ So + Cu2+ + H20

Nordstrom & Southam: Sulfde Mineral Oxidation

375

nlit colonization with Thiobacil1us thioparus under cirumneutral pH conditions

a pH of about 5 with T. ferrooxidans and T. thiooxidans beming preominant
ues of 4 and less. Measured pH is not, however, a unique or acurate indicator of
pulations of thiobacili. Low populations of T. ferrooxidans can be reovere
surface of acidic (pH .c 3) mine talings where evaporation produces low water
hich ca inhibit or kill thobaci11 (Brock 1975, Southam and Beveridge 1992).

at 1991), viable thiobacili ca be cultured from talings possessing neutral

the optimal pH for growth of Thiobacilus spp. is pH .c 3 (Traford et al. 1973,

utal pH values (see Fig. 2; Southam and Beveridge 1992). These thiobacili must
ying acidic nanoenvironments because growth at neutral pH is not possible.

in a gel-like (Hobot et al. 1984) periplasm (Blake et aL. 1992, Harison 1984,

teria-mineral interaction (also see Sand et al. 1995). This close minera interaction
tt because the electron cariers responsible for iron oxidation and energy uptake

entioned previously and shown in Figure 3, growth on mineras is faciltaed by

such as those described by Jones and Starkey (1961). The low Reynolds nu

et al. 1977). A close juncture wil also promote the diffusion of soluble electrn

Uptake of this elementa sufur may be promoted by the production of surface

bacterial-size paricles dictate that diffusion of these soluble constituents away fi

Figs. 1, 2 and 3).

Thobacillus ferrooxidans plotted against

samples from the Lemoine mine tailings

and. Beverdge 1993). The two clusters along

low. pH wher dring has caus deth or

t line are typical of whar is expete for

/Ius spp. The outliers show (1) low populaactivity and (2) high populations ar high pH
acidic nanoen v ironments.

(\

~ 7

E. B

12 6

e 5
'$!

Ji 3

.2 2

from Southam and Beveridge 1992).

ferrooxid and a chalcopyrite mineral surace.

Bar equas 0.5 i. (PubIished with permission

demonstrtes the close association between T.

ings sample from the Lemoine mine which

Figure 3. An unstained thin section of a tal-

pH

2345678

opment of an acidic interfac between the bacteria and the mineral surfaces

low i 978). Colonization of sulfide minerals and the resulting, lithoautotrophy

er bulk 'neutral' pH conditions and probably occurs on the nanoscale through

,g. soluble iron (Fig. 1) or Cu+ (Nielsen and Beck 1972) or atomic % S (Rickard

bacterial cell surface wil be limited (Prcell 1977), promoting continued bacterial ai

ThiQbacilus spp.-mineral interaction in natural systems

Thiobacillus spp. can colonize naturally occurring sulfides (outcrops),
sulfide-containing ore (to promote acid leaching of base metals) and sulfde-beari
wastes (tailings) disposed of, at the earh's surface. The high surface:volume rati

by grinding sulfdes to extract base metas, creates an optimum environment for

Thiobacilus spp. For this reason, the following discussion focuses on the
minerals surfaces in mine tailings environments.
The occurrence of metabolically diverse bacteria in the subsurface (Amy et
down to at least 2.7 km (Boone et al. 1995), suggests that minera sulfdes may

low populations of thobacill prior to mining. Whether or not this is true, mine
become quickly colonize with thiobacili once discharged from the mil (Sout
Beveridge 1993). However, the mechanism of its colonizaon of tailings is
understood (Dispirito et at 1983).
When tailings are deposited as an aqueous slurr and allowed to drain.

at the grain boundares and in the pores between grains because of the
vadose zone, provides all of the essential physical and chemical requirments forgr'

counteracting gravity (Nicholson et a1. 1990). This ara of paral water

Thiobacillus spp. In the vadose zone, the capilar border on the mineral surf:
water to support life (i.e. protetion against dessication which is deleterious to

Brock 1975), the pore spaces allow for the influx of gaseous oxygen (as termnal
acceptor) and carbon dioxide (for carbon fixation) and the sulfide minerals se
substrate for lithotrophy (se Table 2). Dring at the surface of a sulfide tali

freezing conditions reuce thiobacill populations (Southam and Beveridge 1992)

near freezing conditions do not (Ahonen and Tuovinen 1992). Survival ofthiobacil
periodic wetting when microaerophilc to anaerobic environments may form (due
metabolism (Pronk et al. 1992, Das and Mishra 1996).

diffusion of oxygen into water saturated material) is presumably due to

Metallogenium has been described as an organism potentially responsib
transition of minera sulfide-rich environments from neutral to acid pH conditi

and Mitchell 1972). The proper identification of this bacterium is somewhat q

and it is not required for this transition to occur. At the Copper Rand mine l
individual Thiobacil1us ferrooxidans subspecies (an LPS chemotype) w

transform an alkaline pH (pH 8) talings environment down to pH 3 (South

Beveridge 1993). At the Kidd Creek talings pile, Blowes et al. (1995) demons

376
GEOMICROBlOWGY

Thiobacilus ferrooxidans binds preferentially to pyrite dispersed through a

containing abundat organic surfaces (Bagdigian and Myerson 1986, Mustin et

surfaces. These fine grooves (0.2 to 0.5 i) in the mineral surface eventually devel

Bennet and Tributsch (1978) and Norman and Snyman (1987) have demonstrated
ferrooxidans chooses to colonize frcture lines and dislocations on pyritic
corrosion pits, widening and enlarging until the mineral grain is destroyed (Tributsch
NOffian and Snyman 1987). Mineral dislocations may provide convenientp
recesses for bacterial colonization and a unique surface charge promoting the attach
T.ferrooxidans. This is one way in which certain strains may exhibit mineral seleCt

The thiobacilus surface component responsible for preferential binding to

minerals and the resulting close bacteria-mineral interaction is Jipopolysacchaid

because this molecule is situated on the outer membrane surface of Gram-negati

and its side chains extend beyond the usual bilayer strcture of a membrane. n
spp. do not possess capsular material (Shively et al. i 970, Wang et al 1970,
1973, Hirt and Vesta11975, Rodriguez et al. 1986, Yokota et al. 1988). LPS he
(Southam and Beveridge 1993), i.e. differences in LPS Q-antigen side-chains, w

the eel! surface charge character and hydrophobicity which could affect the

different strains to colonize different sulfde mineral surfaces. Because chargee

also pH dependent (Chakabari and Baneijee 1991), the reduction in pH as
colonize mine tailings material would also affect, presumably enhance, their
colonize tailngs as acid mine drainage develops.
Lizama and Suzuki (1991) characterize a T. ferrooxidans strain which COlt

either pyrite or chalcopyrte but not sphalerite and a second strn which co
either pyrite or sphalerite but not chalcopyrite. The abilty to differentiate
chalcopyrite and sphalerite suggests that a form of recognition, presumably re

LPS chemistr (Southam and Beveridge 1993), exists towards these

mechanism is not well understood although it might have something to do with "

Thiobacillus spp. are also known for their ability to adapt to various types of su
prior to the initiation of active microbial leaching (Suzuki et al. 1990). This
by chemical oxidation (Moses and Herman 1991). Although phenotypic switching

demonstrated in T. ferrooxidans, a relationship between LPS chemistr and

1993).

adapatation has not been demonstrated (Schrader and Holms 1988, Southam and 13

Acid mine waters from many different types of oxidizing sulfide mine
have high concentrations of both T. ferrooxidans and T. thiooxid,
roughly equal proportions (Scala et al. 1982). This observation raises the qu
role T. thiooxidans plays in the oxidation process beause 1: ferrooxidans
both iron and sulfur. The difference between 1: ferrooxidans and 1: ihiooxi
simply that T. thiooxidans cannot oxidize Fe(ll. At Brimstone Basin, an

magnitude greater than T. ferrooxidans (Southam, Donald, and Nordstrom,

deposit inYellowstone National Park, T. thiooxidans populations were 2

Nature has selected for the most effcient sulfur-oxidizing bacterium.
Cells grown on ore ar diffcult to dissociate from the ore parcles

Duncan 1974, Suzuki et ai. 1990, Southam and Beveridge 1992) demonstrati
association must occur between Thiobacillus spp. and sulfde mineral
development of a tight association between the bacteria (LPS) and sulfide
proc via a hypothetical two phase mechanism (Southam et aL. 1995). First

salt-bridging or hydrophobic interactions would reversibly attah the b'

minera surface so that an acidic interface could be established to sustain
Phase two encompasses the subsequent cementing of the bacterium to the

Nordstrom & Southam: Sulfde Mineral Oxidation

377

surfaces is supported by their releae after solubilzation of these precipitates

iron oxy-hydroxides (Bigham et ai. 1990, Bhatt et aL. 1993) forming an even more
nanoenvironment (Le. precipitation of Fe(OHh yields H+) to support bacterial
h and multiplication. The role of ferrc oxy-hydroxides in glueing thiobacill to

of1: ferrooxidans.

yet ai. 1988, Southam and Beveridge 1993). Strong adherence of 1: ferrooxidans
oerals via iron precipitates (Southam and Beveridge 1992, 1993) may have an
:at ecological role in reducing the diffusion of metabolic products (e.g. Fe(III) and
ic acid) away from the cell-mineral interface. This would help maintain an acidic
nvironment at the mineral surface and provide a potential source of soluble ferrous
rough repeated chemical oxidation of the sulfide (Reaction 2) thereby promoting the

of temperature

f ternperature from OC in some waste rock piles (Strmberg and Banwar 1994), to

vironments where iron, sulfur, and sulfide mineras are oxidizing can have a large

also determne the predomiant genus and species. Bacteria ar theimly divided

Cin some underground mines (Nordstrom and Potter 1977, Nordstrom and Alpers
d waste rock piles (Hendy i 987), to boiling in hot spring waters (Bott and Brock
eIIperature is one of the distinctive and most importt environmenta parameters
ences the activity of microorganisms. It not only influences their rate of growth

chrophiles, mesophles, thermophiles and hypertermophiles. Psychrophiles can

0 with an optimum of 10-15 and a range up to 30C. Mesophiles tend to grow at

lures below 40C with an optimum temperature around 30C. Thermophiles have an
temperatue of about 50 -6C and hypertermophiles have an optimum
lure of;;80C, Both obligate and facultative thermophiles have also been observed.

little information is available on psychrophiJc activity in mine waste environments

perature rage of if to 12C and averaging 5C, microbial cataysis is afecting

berg (1997) has provided evidence that for a waste rock pile at Aitik, Sweden

ation. Ferroni et al. (1986) and Bertelot et al. (1993) found that speies such as
'das can be psychrotrophic. They enriched mine water samples from Elliot
rio and found that growth continued at temperatures as low as 2C, with faster

r the enrched mine water than that for 1: ferrooxidans ATCC 33020. Both

ad the same growth rates and the same optimum temperare over the range of 12

ws the temperature range for growth of several important mesophles and

hilc iron- and sulfur-oxidizing bacteria are either mesophiles or thermophiJes.

es (Norris 1990). The growth rates shown ar not neessarily independent of

is (1990) has noted the increase in rate with an increas in pH for T.

ans. However, Nordstrom (1977, 1985) found that the ferrous iron oxidation
pH 1-2 was virtually the same as that for 9K culture medium of

iie influence of pH on microbial kinetics has not been clearly defined for sulfide

.cdifne waters of

and. ferrous iron oxidation. Thiobacilus spp. and Leptospirilum spp. ar

with tyical temperature optima in the rage of 30 to 35C, although the same
have a different range and optimum as shown in Figue 4. These species have a

where pyrite is oxidizing. The new species, Leptospirilum

range that coincides well with the typica temperature range of most

'ooxidans, is a moderate thennophile with a temperatre optimum of 4SO-500C

hological variation and are more elongated (Karvaiko et al. 1988).

va et al. 1992). Sulfobacilus thermosulfdooxidans and stran THI are Gramermophiles, and facultative Jithotrophs, unlike 1: ferrooxidans. They show

378

::

~
i

.i0

10

20

:;E is
.5

::

"0
c:

0
35

.2 25
1I

"0

1(
c:

-0..
10

..

GEOMICROBIOWGY

0
tJ

It
A.

50

1
D

1.0

30

+
v

20

T. ferrooxidans. (Ha

T. ferrooxidans 0
T. ferrooxidans os
Leptospirilfum (6
Moderate thermop
Moderate thermop

60

70

80

Sulf%butS (lMst

Temperature, "(:

thermophles (reproduced with permission from Norrs 1990).

Figure 4. Temperature rages for severa acidophilic iron- an sulfur-oxidizing m

Fe2+

There ar four genera of Archaea that iie aerobc, acidophilc, cocoid in

moderate to extrme thermophiles: Sulfolobus, Acdanus, Metallosph
Sulfrococcus. They oxidize reduced sulfur compounds and some oxidize

and 70C.

minerals. Thermophiles that oxidize iron and sulfur ar Sulfolobus spp.and

spp. Since the original classification of Sulfolobus acidocaldarius by Brocket
thre speies have been recognize: S. acidicaldarius. S. solfataricus,and
(Zilig et al. 1980). S. brierleyi has subsequently been reclassified as Acidian
Sulfolobus oxidizes arsenopyrite as wen as pyrite (Ngubane and Baecker 1
and Parot (1986) have demonstrated the cataytc effect of Sulfolobuson the
concentrates of pyrite, chalcopyrite, pentlandite, and nickeliferous pyrrtite
As previously described, Thiobacilus spp. ar Gram-negative. Ba

possessing LPS as their outermost cell surfac component (Fig. 1, Berri

1982; Fig. 6). An S-layer is a two-dmensional paracrystaline aray

while Sulfolobus spp. only possess an S-layer external to the cell mernbran
functions as a diffusion barer in cells on which they occur (see by p.

which is responsible for the growth of Thiobacilus spp. on minera s

volume). For Sulfolobus spp. the formation of a nanoenvironment scale di

must be accomplished without a periplasm. The same must be tre for

Thennoplasma acidophilum (see next section).

Nordstrom & Southam: Sulfde Mineral Oxidation

379

(left. A stae thin-section of Thiobadllus ferrooxid ATCC 13661 demonstrting the

-negative cell envelope strcture in which lipopolysacchardes reprent the outermost envelop
. Br equals 50 nm.

(right). A negatively staned Sulfolobus spp. demonstrting the crystaline nature of the cell
r equals 200 nm.

d Deryugina 1963) is likely a Sulfobacillus spp. (Golovacheva and Karavaiko

on its ability to produce bacterial endospores, Thiobacillus thermohilca

am-positive, acidophilic iron-, sulfur- and mineral-oxidizing bacteria have not

ery much atention. The fact that they ar not common, or at leat raely
may relate to the diffculty with which a Gram-positive baterium can establish
diffusion grdient

review of the literate on bacterial physiology and bacterial interactions with

iron- and sulfur-oxidizers but dominate by the Arhae at the higher

eras we have tred to show how Thiobacillus spp. function at low pH and
feme iron from ferrous. At the physiological level, the promotion of sulfide
dation by bacteria does not require their attachment to surfaces but the close
ld certainly decreae the diffusion distance to the substrate source thereby
higher concentrations of iron for growth. The overall effect is to enhance the
.t.High temperature (40 to 100C) oxidation is also enhance by both Bacteria

ROBIAL ECOLOGY IN MINE WASTE ENVIRONMENTS

trduction to this chapter we mentioned that mine waste environments and acid
support a wide diversity of microbial Hfe. Autotrophic bacteria, heterotrophic
algae, fungi, yeasts, mycoplasmas, and amoebae have all been found in acid
. A study by Wichlacz and Unz (1981) reported 37 acidophilic heterotrophs
en

us heterotrophic bacteria in association with coal refuse piles. In the Rum

lated and pary charterized from acid mine drainage. Belly and Brock (1974)

he, Australia, a mine dump was found to have relatively low numbers of T.

gesting a stable population had been established (Goodman et aL. 1981). The

and high numbers of acidophilic heterotrphs with no apparent seasonal

f this rich and complex microbial ecology deserves a short discussion.

380
GEOMICROBIOWGY

As Dugan et ai. (1970), Johnson et ai. (1979), and Ledi and

astutely pointed out, autotrophic thiobacill wil leak or excrte organc compo

be utilize by heterotrophic bacteria. De autotrphic cell wil provide

sustenance for heterotrophs. Furermore, a commensa re1ationship,poss
symbiosis (Battahara et aL 1990), exists between heterotrphic and

bacteria. T. ferrooxidans excretes pyrvate dunng its grwth (Schnaitman

1965) and pyruvate can inbit growth. The heterotrph Acidiphilum
pyruvat as a can and energy source and its prsence can enhance th

common inhabitats of acid mie drainage (Harson 1981, Wichlac

ferrooxidiis (Harson 1984, Wichlacz and Thompson 1988). Acidiphil.

Kishimoto and Tano 1987) and coppr dump leahig operations (Groudev

1993) and they ar aiways found in assoiation with T. ferrooxidaiis (L

Bhatthara et al. 1991).

Ehrlich (1996) and Le and Pedersen (1996) have note thatse

microorgansms live in close assoiation with T. ferrooxidans. Some of
speies of thobacill not previously (see Table 1). Oter heterotrophic mic

beside Acidiphilum spp., include Pseudomonas, Bacillus, Micrococc.

Crenothrix, Microsporium, Aerobacter, CauIobacter, and the fungi and yeas

Cladosporium Penecillum, Trichosporon, and Rhodotorula. Brock (1973)
that the lower pH lit for the growth of cyanobacteria (formerly "blue-gr

about 4 and only grn algae can tolerate lower pH conditions. Green algae ar
acid mine waters where they have acs to sufcient sunlight and contiuous

flowing water. Nordstrom (1977) found several types of grn algae at Iron

ChIorella Ulothri, Chroomona, and Euglena. Addtional acidophiic or

Californa. The most common algae occurg in acid mine waters ar Chlai

algae, diatoms, and higher plants are described in Kelly (i 988).

One of the most unusual microorgansms found in envirnments wherepy

is the Mycoplasma, Thermoplama acidophilum (Darland et al. 1970). Myo
like bacteria without cell walls. They ar Gr-negative, highly pleomorpc
organisms, and yet T. acidophilum has a pH optimum of 1-2 and a temper
of about 60C.
The microbial ecology of environments where acid waters have develo~

oxidation of pyrite and other sulfide mineras is poorly understood. Investigati

shown the possibilty for a microbial succsion from autotrophs to heterotroph

complex organisms in a food chain. If the hydrology and clima do not have
large varatons (e.g. steady-sta flow most of the time) there ar better opp
growt of a stale and more mat microbial community. Those envirnments

varable and dynamc conditions (high erosion rates, onset oT sudden ex

should discourage the development of large and stable populations of microbes.

SUMMARY AND FUTURE WOR.K

Any attmpts to understand the degradation of pyrte and other sulfde mie

without reognizng the role of microorganisms ar likely to faiL. Literatu on the

ameliora the water quality hazds associated with mig of sulfide minera
voluminous. More than a centu ago, microbial interactions with sulfur and
mineras have ben scientificay investigated Lithoautotrophs, such as Thio
jerrooxidans, Thiobacillus thiooxidans, Leptospirilum ferrooxidans, and some
co-habitats such as Acidiphilum, Thrmoplasma Bacillus, Micrococcus, Ch

Nordstrom & Southam: Sulfde Mineral Oxidation

381

'horella Ulothrix, and Euglena ar an integral par of the environment where

'nerals ar oxidizing.

'gations on the geomicrobiology of sulfide mineral oxidation have clarfied the

y attak the sulfde suiface. These rates are comparable so that pyrite wil oxidize

of microbial cataysis, physiological features that allow them to respire and

in acidic waters, and their microbial ecology. The main role of iron- and sulfurI:acteria is in the oxidation of aqueous ferrous to ferrc iron. The ferrc iron can

ernc iron as rapidly as the microbes can regenerate the ferrc iron. The bacterial
of ferrous iron, however, wil be a function of environmental conditions including

on, ecology of commensal or predatory species, oxygen concentrations,

nIy) temperature, pH, density or tota dissolved solids, chemical composition of

itiaton of pyrite oxidation does not require an elaborate sequence of different

ic conditions, and mineralogy.

gtessive oxidation, the nanoenvironment (nanometer scale) beomes a

al reactions that dominate at different pH ranges (e.g. Kleinmann et al. 1981).

Jus spp. employ nanoenvironments to grow on sulfide mineral suraces, usually
ted biofims (Southam et al. 1995). These nanoenvironments ca develop
sof acidic water that, at first, d not afect the bulk water chemistr. Eventually,

ironment (micrometer scale). Evidence for acidic microenvironments in the

of circurneutral pH for the bulk water in the subsurface can be found in the

Jarosite can only form under acidic conditions. The occurrence of isolated

of jarosite in certain soil horizons where the current soil water is neutral (Carson

goethite pseudomorphs afer pyrite also suggests that pH gradients probably

experiments such as those of Goldhaber (i 983) and Moses et aL. (1987) indicate

ar the suiface of the oxidizing pyrite but may not have affected the bulk watr
urse, the bulk water may have been acidic in the past and currently it is neutral,
dimensions at the mineral-water interface.

of oxidative chemistr with large chemical gradients occur within nanoscale to

of the contradictory studies regarding bacterial adsorption on sulfide surfaces and

Oed" The varous factors that can inhibit autotrophic growth in sulfide mineral

n and importce of Sulfolobus and Sulfobacilus in mine waste environments

t on oxidation rates need to be resolved. The mechanism of T. ferrooxidans

selectivity is not known, however, it must be conferred by the nature of its
accharde. The Sulfolobus minera interface has not been studied, nor ha.~ the

nts and their relative importance should be clarfied.

oxidation of elementa sulfur by Thiobacilus spp. requires the formation of a

agent that reduces the surfac tension. Jones and Starkey (1961) describe a
eous compound which promotes growt of T. thiooxidans on elementa sulfur.

"ng agent is also importt for dissolution of the sulfur-rich layer formed by acid
of bas metas from pyrite and chalcopyrite. In his review of the biochemistr of
sulfur oxidation by chemolithotrophs, Kelly (1982) emphasized the oxidation of
te and polythionates with almost no information on solid sulfur oxidation. Clearly
dies are needed to elucidate the mechanism of growth on elementa sulfur.

robial ecology and phylogeny have undergone a revolution with the application of
A sequence analysis. However, defining phylogenetic relationships based on
ediversity raises new problems that have yet to be addressed, such as how to
l conventional taonomy based on physiology and function with differences based
types. Recnt work on thobacill have highlighted some of these diffculties
and Stackebrandt 1994). Although strain-speific molecular probes may not be

382
GEOMICROBJOWGY

possible, the phylogenetic diversity of Thiobacillus spp. has ben reVeaed\vith

sequence analysis (Lane et al. 1985, Gobel and Stackebrandt 1994). This

diversity has enabled the use of 16S rRNA probe (Goebel and Stackebrandt

PCR-mediated 168 rDNA detection (Wulf-Durad et ai. 1997)

microorganisms from natal environments and bio-leaching
developments in microbial ecology of acidophilic microorganisms wil
molecular techniques.

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GEOMICROBlOWGY

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Thiobacillus thiooxidas. a new sulphur-oxidizig organsm isolated from the soiL. J

Wakman SA. lfe is (1922) Microorganisms conceed in the oxidation of sulphur

256

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of

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125:259-269

EO

Chapter 12

CHEMICAL WEATHERING OF SILICA l'E

illam W. Barker, Susan A. Welch and Jillian F. Banfield

Department of Geology and Geophysics

Weeks Hall, 1215 West Dayton Street
The University of Wisconsin-Madison
Madison, Wisconsin 53706 U.SA

INTRODUCTION

enormous body of increasingly interdisciplinar scientific literature reflects the

ound and pervasive entwinement of biological processes and silicate mineral

ochemically mediate cycles:

ering. \Vhile the geomicrobiology of silcate minera weathering might seem an

mdy arcane subject, consider the following short list of processes affected

of architectual materials

Soil formation and plant nutrition

Geochemistry of groundwater and movement of contaminants

Long term stability of geological nuclear repositories
Effects of mineral weathering on climate on a geological time scale

6, Jones 1988). Weathering of minerals in soils releass major nutrients such as K, P,

scientists are concemed with pedogenesis, the process of soil formation, and recognize
central role of organisms in mineral weathering (see, for example, Huang and Schnitzer

tnutritionists, primarly working with model rhizospheres, have documented the

Ca, Mg, Si, as well as trace ions which are necessary for microbial and plant growth.

atic and astonishingly rapid biomobilzation of essential nutrients from phyllosHicates

singer et aL. 1992, Leyval and Berthelin 1991).

Engineers and conservationists, concerned with the long term stabilty of architectural

terials, have contributed greatly to defining communities of organisms and the damage
y cause to natural and synthetic building materials. Severa investigators (D la Torre et
1993, Eckhardt 1978, Krmbein et al. 1991, Palmer et a1. 1991, Sand and Bock 1991,
iet a1. 1991) have focused on the biological weathering of stone building material and

ass, and have demonstrated enhanced corrosion and weathering of these materials

sodated with attached organisms, presumably due to the production of addic, alkaline,
comp1exing compounds which would enhance the dissolution of the solid substrata.

eral weathering, both in a natural and architectural context. Easton (1994) reviewed the

rvittori et al. (1994) published an excellent review on the role of lichens in rock and

.erature from a geologist's perspective.

recognzed, similar processes also occur n subsurface environments. Recent

While microbial weathering of minerals in soils and structures at the Earh's surface is

mbers (approximately 105 to 107 cells!cm3), Microbial abundance and diversity is

rveys of deep subsurface aquifers (hundreds of meters), show relatively high microbial

Holm et a!. 1992) where they can directly impact mineral surface chemistr, water

able but does not decrease systematically with depth (Balkwil 1989). While some
teria are free living in solution, most OCCur attached to mineral surfaces (Hazen et aL

0275-0279/97/0035-00 12$05 .00

390

GEOMICROBlOWGY

Walman SA, Jfe JS (1921) Acid production by a new sulfu-OlUding bacterium. Science 53:216
Walman SA, Jfe JS (1922) Microorganisms coered in the olUdation of sulphur in the...s
Thiobacilus thiooxida, a new sulphur-OJdizing organsm isolate from the soiL. J Bacteriol i
256

pH 2.0. Ca Mineral 24:35-4

Walsh AW, Ritidt JD (1986) Rates of reaction of covellte and blaubleibender covellte with ferrc'
Walsh F, Mitchell R (1972) An acid'olerant iron-oxidizing Metallogenum. J Gen Microbiol72:369-3

Wichlacz PL, Thompson DL (1988) The effec of acidophilic bactlna on the leahing of co
Thiobacilus ferrooxida. In: PR Norrs, DP Kelly (ed) Biohydrmetaurgy, Proc IntI Symp!
Warick, UK. Science Tech Lettrs, p 77-86, Kew, UK
Wichlacz PL. Unz RF (1981) Acidophilic, heterotrophic bateria of acidic mine waters. Appl Bnv'
Microbiol 41: 1254-1261
drainage. Inti J Syst Bacterio136: 197-201

Wich1acz PL, Unz RF. Langworty TA (1986) Acidiphilu11 angustum sp. nov., Acidiphilum fac/is
nov., Acidiphilum rurum sp. nov.: acidophilic heterotrophic bateria isolated from acidic coal

Wiersa CL, Ristidt J D (1984) Rate of reaction of pyrte and marcasite with ferrc iron at
Geohi Cosmochi Acta 48:85-92
Williamson MA Ristidt il (1993) The rate of decomposition of the ferrc-thosulate complex in
aqueous solutions. Geohi Cosmochi Acta 57:3555-3561

Chapter 12

JiHian F, Banfield

IOGEOCHEMICAL WEATHERING OF SILICATE MINERALS

Willam \v. Barker, Susan . Welch

Madison, Wisconsin 53706 US.A.

Department of Geology and Geophysics

Weeks Hall, 1215 West Dayton Street
The University of Wisconsin-Madison

INTRODUCTION

An enonnous body of increasingly interdisciplinar scientific literature reflects the

found and pervasive entwinement of biological processes and silicate mineral
athering. While the geomicrobioJogy of silicate mineral weathering might sem an
geochemically mediated cycles:

trmeJy arcane subject, consider the following short list of processes afected

Stabilty of architectural materials

Soil fonnation and plant nutrition

Woo AP, Kelly DP (1991) Isolation an charterization of Thiobacillus halophilus sp. nov., a

Winogradsky SN (1888) br Eisenbakerien. Bot Ztg 46:261-276

156:277-280

t nutritionists, primarly working with model rhizospheres, have documented the

are concerned with pedogenesis, the process of soil formation, and recognize
central role of organisms in mineral weathering (see, for example, Huang and Schnitzer
86, Jones 1988). Weathering of minerals in soils releases major nutrients such as K, P,
, Ca, Mg, Si, as well as trce ions which are necessar for microbial and plant growth.

Geochemistry of groundwater and movement of contaminants

Long term stablty of geological nuclear repositories
Effects of mineral weathering on climate on a geological time scale

OlUdizing autotrophic eubacterium from a Weste Australan hypersaline lake. Arch Micro
Yakontova LK. zeman I, Nesterovich LG (1980) Oxidation of tetredte. Doldady, Ear Sd Sect,

Nauk SSSR 253:461-464

Yin Q. Kelsall GR, Vaughan DJ, Englund KER (1995) Atmospheric and electrochemical oxidation of
surface of chalcopyrite (CuFeS2). Geochi Cosmochim Acta 59:1091-1100
and Thiobacilusferrooxidans. J Gen Appl Mcrobio14:27-37

Yokota A. Yam Y, Im K (1988) Lipopo1ysachardes of ron-oxidizing Leptospirilum

Zillg W, Stette KO. Wundel A. Schulz W, Press H, Scholz I (1980) The Sulfolohus
group: Taxonomy on the basis of the strcture of DNA-depndent RNA po1ymeraes. Arh
125:259-269

insinger et at 1992, Leyva! and Berthelin 1991).

'amatc and astonishingly rapid biomobilzaton of essential nutrients from phylJosilcate

Engineers and conservationists, concerned with the term stability of architectural

ierials, have contributed greatly to defining communities of organisms and the damage
to natural and synthetic building materials. Several investigators (D la Torre et

Eckhardt J978, Krumbein et al. 1991, Palmer et at i 991, Sand and Bock 1991,

et a1. 1991) have focused on the biological weathering of stone building material and
and have demonstrated enhanced corrosion and weathering of these materials
with atched organisms, presumably due to the production of acidic, alkaline,
complexing compounds which would enhance the dissolution of the solid substrata.
ittori et al. (1994) published an excellent review on the rote of lichens in rock and
neral weathering, both in a natural and architectural context. Easton (1994) reviewed the
rature from a geologist's perspective.

microbial weathering ofminerais in soils and strctures at the Earh's surface is

recognized, similar processes also ocur in subsurface environments. Recnt

rveys of deep subsurface aqufers (hundreds of meters), show relatively high microbial
umbers (approximately 105 to 107 cells/cm3). Microbial abundace and diversity is

ariable but does not decrease systematically with depth (Balkwil J989). Whle some

Holm et at 1992) where they can diretly impact mineral surface chemistry, water

eria are free living in solution, most occur attahed to mineral surfaces (Hazen et at

0275-0279/97/0035-00 12$05.00

GEOMICROBlOLOGY

Barker, Welch, Banfield: Biochemical Weathering of Silcates

393

ations of organic and inorganic acids. It is diffcult to extrapolate from these high nutrent

392

xperiments to estiate the magnitude of this effect in nature, where minera weaering

ict the magnitude of any observed effects under field conditions.

actions. It is unclear whether one can extrapolate those results to natura systems and

periments we can detemne whether or not microorganisms can afect geocheITcal

tential, temperatue and light levels. Based on the results of these types of laboratory

organisms which ca grow in culture, and therefore may not accurately represent the
ibution of microorganisms and complex biogeochemical processes occurring in nature.
itional natural varables which are diffcult to simulate in vitro ar fluctuations in water

'ments tyicaly use a single strn of bacteria or else an assemblage of

laboratory weathering experiments are in suspension, where any dissolution enhancing

abo1ites produced would be diluted by the bulk solution. Laboratory mineral dissolution

As.. previously mentioned, bacterial distributions in natural environments ar typically

heterogeneous and most are atthed to mineral surfaces. In contrast, most bacteria in

rates, organic carbon, and nutrient concentrations, are typically orders of magrutude lower.

rock interaction, and groundwater geochemistr (Bennett et aL. 1996, Chapelle 1993
1962, Hiebert and Bennett 1992, Lovely and Chapelle 1993, McMahon et al. 1991, 1992).

Chapl1e et aL 1987, Chapelle and Lovely 1990, Fyfe 1996, Ghiorse 1997, Gurevich

Atthed microorganisms ca etch minera surfaces, releasing ions to solution (Bennett ei

aL. 1996, Hiebert and Bennett 1992), and also serve as nucleation sites for a varety of
seconda mineral phases (Ehrlich 1996, Ferris et aL. 1988, 1989, 1994; Konhauser et.al.

1994, Konhauser and Ferris 1996, Schultze-La et al. 1992, 1994, 1996). Microbial
redox processes in aquifers can directly affect the distribution of elements such as C, 0, N
Fe, Mn, S, As, U (Herrng and Stumm 1990). These in tum can have indirect effects oii
other geohemical reactions. For an extensive review of groundwater biogeochemistr, se

Chapelle (1993).
Environmentally acptable sequestration of nuclea waste materials over period
time approaching geologica scales forms one of the most pressing environmental proble
of modem society. Currently, vitrification, encapsulation of radioactive materials in a gl
matrix, and storage in underground repositories appear to be the most politically ex ..

course of action. In these environments, parcularly over the long periods of time

Extensive field evidence exists for microbially-medated minera weathering on rock

tfaces and in soils, aquifers, and the marine environment. Natural microbially medated

to safely ensure storage, groundwater and its associated microorganisms may inter:

the glass surfaces, releasing ions (possible radioactive) to the environment. B

colonizing minera surfacs in aquifers, as mentioned above, preferentially etch att.

'neral weathering reactions have been investigated by direct analysis of ITneral surfaces
dathed microorgansms using light and electron microscopy. Microbially enhanced

carbonates (Berner et al. 1983). Becuse microorganisms may have afected bioge

1996) showed that feldspar and quar weatering in a shallow aquifer increased when

crocosm studies (Bennett and Hiebert 1992, Hiebert and Bennett 1992, Bennett et aL.

portt role in mineral weatering and geochemical cycling of elements. In situ

Bacteria are ubiquitous in the Ea's surface and subsurface environments and play an

'neral solutes and microbial metabolites.

inera weathering has also been detemned indirectly by analyzing natural waters for

surfaces and are well known to have the abilty to solubilize glass (Staudigel et al. 1995
At some point in the future, if and when water and subsurace lithotrophic microbes inter
with the vitnfied waste, release of radioactive contanants wil occur.

Global warng due to accumulation of CO2 in the atmosphere constitutes anoth

serious environmenta problem. A major feeback mechanism controllng atmospheri
chemical weathering reactions for at leat 3.8 Ga, the biota could have moderated theC2

acteria colonized mineral surfaces, even when solutions were supersaturated with respect
o the dissolving phase. Many etch pits seen on mineral surfaces approximated the size and

pC02 is the weathering of Ca-Mg silcate and subsequent precipitation of Ca-M

Si cycle, and could have therefore affected pC02 and global climate (Gwiazdaan
Broeker 1994, Schwarzman and Yolk 1991).

pe. of bacteria colonizing minera surfaces, and the authors hypothesized that atthed
furia locally increased mineral dissolution rates by creating a micro-reaction zone of
'ganic acids and other metaolites concentrated at the mineral surface. Thorseth et al.

s to solutions (Bennett and Siegel 1987, McMahon and Chapelle 1991, McMahon et
1992).

ic acids in aquifers has ben cited as a mechanism for the release of solutes frm

irrlation between mineral solutes and microbial metabolites in solution. Berthelin et aL

985) found a nearly 1: i correlation between cations releasd to solution and nitrate
ncentration in soil, indicating that bacterial nitrification releases minera catons to
. on by ion exchange and proton promoted mineral dissolution. Baceral production of

mpellng as finding a bacterium in a bacteria-shaped etch pit, there is often good

While evidence for bacterially mediated weathering of silcate minerals is not always as

ble bacteria actively altered glass surfaces.

ghly alkaline microenvironments. Bacteria can also playa role in the alteration of silicate
inerals in marine environments. Thorseth et al. (l995a,b) examned glass rims of pilow
vas from oceanic crust. Once again they found microbe sized etch features, in this case
oritaining DNA. The basalt chemistr had been altered in zones immediately surrounding
etch features and potasium was enriched within the microbial etch pits, indicating that

rfces. In this case, however, they atibuted enhanced weathering to production of

1992) found similar etch strctures associated with coloruzing cyanobacteria on palagonite

METHODS

Lab studies
Experimental studies of the effects of microorganisms on mineral weathering rates
reactions are commonly performed in either closed (batch) or open (flow-through) reaction
vessels. In batch experiments, mineras and solutions ar placed in a container, solution
composition is monitored over time, and reaction rates ar caculated from the evo1utionor

solution chemistry. In flow through experiments, solution passes through retion vessels
containing mineral samples and reation rates ar caculated from effuent concentration

flow rate. Mineral weathering rates detemned in vitro typically exce those derivedf:

field-based measurements by one to three orders of magnitude, because these controll

laboratory experiments cannot simulate the more complicate water-rock interactionsi

1990). Whle diffcult to predict the absolute magnitude of a reaction, one may de

natural environments (Brantley 1992, Swoboda-Colberg and Drever 1992, Velbel 198

effects of microbial metabolites on weathering reactions.

When these types of experiments include microorganisms, unrealisticallyhig

concentratons of organic carbon and nutrents are added to solution (Avakyan et aL i 981

1985, Bertelin and Dommergues 1972, Bertelin i 971, Karavaiko et al. 1984, 1979;
Kutuzova 1969, Malinovskaya et al. 1990, Vandevivere et al. 1994). Microorganis

often significantly enhance minera dissolution rates in vitro by producing high concen

394
GEOMICROBlOLOGY

Abundat field evidence for fungal mediation of mineral weathering also exists, thou
most of this comes from literare on weathering of architectual materials (D Ia Torr
al. 1993, Hirsch et al. 1995, Krmbein et al. 1991, Palmer et al. 1991, Palmer and Hi
1991, Sand and Bock 1991, Urz et al. 1991). Bacteria and fungi commonly coexist

and
is difficult to distinguish between bacterial and fungal weathering of silicates. Fungi may
more important than bacteria in microbially-mediated weathering as they produce an

rock

excrete higher concentrations of more effective dissolution enhancing ligands (Palmertal

1991). But fungi are not as abundant as bacteria in most environments and do not occuriii
some extreme environments where bacteria flourish. Algae are also common on

surfaces and can influence mineral weathering reactions though they ar usually conside

to be less effective than bacteria or fungi (Ortega-Calvo et al. 1995). Wh1e algae may n
significantly impact mineral weathering reactions, they do provide a carbon rich substrat,
for both bacteria and fungi.
In lichens, gren algae and/or cyanobacteria (phycobiont) form a symbiotic (Ns
1996) or "controlled paritic" (Ahmadjian 1995) relationship with fungi (mycobiol1t.

While a host of other organsms such as rotifers, protozoa, diatoms, bacteria, unlichenized
cyanobacteria and fungi, tardigrades, arhropods, and gastropods inhabit these lithobio1tic
(Go1ubic et al. 1981) communities, most biogeohemical weathering researh has fOCUsed

on the lichen component.

Lichens aggressively attack mineral surfaces, resulting in both physica (Fry 1927)
chemical weathering of rock surfacs (see reviews by Easton 1994, Jones 1988, Piervi
et al. 1994). Early researchers used light microscopy to document extensive disaggreg
of minerals and binding of the resultant pariculate by lichens to form "organomineral

(Fry 1927). With the application of X-ray diffraction (XR) and scanning elec

microscopes (SRM) equipped with energy-dispersive X-ray microanalysis (EDS),

researchers documented strongly etched mineral surfaces beneath lichens (Jones et aL.
1980, Jones et al. 1981) as well as meta oxalates whose cationic character clearly mirrored

that of the mineral substratum (Chisolm et al. 1987, Purvis 1984, Wilson et ai. 1980,
Wilson and Jones 1984). Recent research applied back-scattered electron (BSE) imaging
study biodeterioration of minerals by Hthobiontic microorganisms (Ascaso and Wierz
1994, Ascaso et al. 1995, Barker and Banfield 1996, Sanders et at 1994, Wierzhosan
Ascaso 1994, 1996).

While these studies ar important in understanding the relationships between licheiiS

and minerals, the reactions which charterize mineral transformations take place at a scale
beyond the resolving power of SEM. A high-resolution transmission electron microscope

(HRTEM) provides simultaeous strctual information via selected area electrqo

diffraction (SAED) and chemica data though EDS. Thus, it is an ideal instrument with.
which to study biogeochemical mineral transformaton reactions at the subnanometer scale.

Diffculties inherent in producing samples suffciently thin for TE analysiswh

preserving the intat organic-mineral interface have limited its application. Reee

developments in energy fitered transmission electron microscopy (EFlEM) have made

possible to not only collect zero Joss images of exceptional clarty (chromatic aberration
eliminated by the energy filter) and contrast (without using contrast-enhancing heavy
stains), but also electron energy loss (EELS) images that detail elemental distributionsafth
nanometer scale.

While TE has ben used to characterize minerals extracted from Iichens,rn

preparative methods employed to date involve scraping the mineral grains accumulated
the lichen-rock interface free from the thallus, and removing the organic component wi1
oxidaton in H202 and ultrasonication. These techniques destroy all textura informatioii

and drastically alter the mineralogical component (Birrell 1971, Cook 1992, Douglas and

Barker, Welch, Banfield: Biochemical Weathering of Silcates

395

ntly, Ascaso and Ollacarizqueta (1991) reported limited success in an attmpt to apply

essinger 1971, Lakvulich and Wiens 1970, Perez-Rodriguez and Wilson 1969).

ogical and physical sample preparation techniques to examne the intat organc-mineral

d knife ultramcrotomy to study the interface of lichens and a marble building stone.
ker and Banfield (1996) and Wie17.chos and Ascaso (1996) used a combination of

rfac by a varety of electron microscopic techniques. Such diret comparisons of

siochemical and biogeohemica weathering of silca minerals by microorganisms

prising lithobiontic communities on outcrops of known exposure age allows both

chanisms and rates to be determined from field observations.

MECHANISMS

The following biological processes are commonly cited as explanations for increasd
kate mineral weathering.

reactions to occur.

(1) Growing roots and fungal hyphae physically disrupt minerals, exposing new
fresh mineral surfaces and increasing surface area available for reaction.
(2) Soil stabilzation increases water retention, lengthening time for weathering

authigenic mineral formation.

(3) Acid production, primaly carbonic acid from CO2, but also other inorganic
and organic acids, accelerate weathering rates.
(4) Organic ligands directly attk minera surfaces or form complexes with ions
in solution, changing saturation state.
(5) Complex extracellular polymers moderate water potential, maitan diffusion
channels, act as ligands or chelators, and serve as nucleation sites for
and enhances weathering.

(6) Nutrient absorption, primarily K, Fe and P, decreases solution saturation state

hysical disaggregation

ggregate rock surfaces, is perhaps the most strikingly obvious biological process

The ability of microorganisms, parcularly lichen communities, to physically

olved in silicate mineral weathering (Fig. 1). This physical disaggregation of minerals
reases mineral surface area and exposes new fresh mineral surfaces for biogeohemical

regation is only fully appreciate when one views an optical thn section across the

weathering. When one views a thin section across the intact mineral-lithobiontic community
interface, for example the sheer physical disruption reuired to produce such shattere
mineral grains is the most immediately impressive aspect of these organomineral interfaces
arker and Banfield 1996, Wierzhos and Ascaso 1996). The tre extent of biophysical

and colonize mineral substrata as soon as the space becomes available. The

mineral interfac using backscattere electron imaging. Microorganisms aggssively

hanisms involved in biophysical disaggregation of minerals are not well understood.

For rock surfaces, freze-thaw and subsequent colonization of frehly exposed minera
surfaces along grain boundaes and cleavages is probably an importnt mechanism. While

xplanation for shattered rock surfaces, apparently no one has ever measured forces which

'orces generated by the altemate wettng and drying of lichen thalli are often cite as an

'ght be generated by these hydration/dehydrtion cycles. Griffn (1981) points out that the
availabilty of water works in concert with the physical pore size to control the distribution

of microorganisms in nonsaturated environments, most commonly soils and on rock

surfaces. Whle bacterial movement is much more limite by falling water potential

(Papendick and Campbell 1981) than that of fungi (Griffn J 981), the later reuire much
larger passageways in rocks and soils. Rhizosphere studies comparing mineral weathering

396
GEOMICROBlOWGY

Figure 1. Backscatt electrn micrograph of the intact interface between the lichen Porpidia

albocaerulescens and metasyenite. Fungal hyphae have penetrated along grain boiindaes and cleavages to
extensively disaggregate the rock surace (Barker and Banfield 1996).

by roots, roots plus associated symbiotic microorganisms and roots plus symbionts plus
other rhizosphere organisms demonstrate a strong corrlation between K releae from
biotite and phlogopite for the latter group, attibutable to "better soil exploration" (Bertelin
and Leyval1982, Leyval and Berthelin 1991).

SoH stabilzation

both plant and microbial carbon compounds (Oades 1993).

It has ben suggested that the most critical factor affecting the biotic enhancement of
weathering is the stabilzation of soils (Drever 1994, Schwaran et aL. 1993). There is a
strong positive correlation between soil stabilization and organic content, although this
organic content is comprised of

Roots of higher plants stabilize larger soil aggregates, and provide channels for water and
oxygen to reach soil paricles. Fungal hyphae physically bind soil paricles together as well
(Forster and Nicolson 1981a,b). These ectomycorrhyza fungal hyphae dramaticaly

Barker, Welch, Banfield: Biochemical Weathering of Slcates

397

Figure 2. Kaolinite (K) enmeshed in the aruonic mucopolysacchaide (P) capsule of Klebsiella
IIcrograph (Barker 1988).

pneumoniae (B). Ruthenium re-stned diamond knife thin section, bright-field transmission electron

increase contact area between biological and inorganic mineral surfaces, enhanciiig

exposure of minerals to corrosive substances (water and metabolites). Interpariculate

bridging of soil minerals by extracellular polysacchardes (Fig. 2) is a major component of
soil aggregaton (Tisdall 1994). Polymers that have high concentration of acid functional

groups, primarly uronic acids, are most effective for enhancing sediment stability (Dade et

al. 1990). Whle the aggregation of soil parcles by plants and microorganisms decreae

physical weathering rates, increased soil surface ar and water residence time increa

chemical weathering. Microbial colonization and stabilizaion of soils is a crtical

preliminary step for colonization of surfaces by higher plants (Forster and Nicolson
1981b).
Inorganic acids

Silcate miera dissolution is a complex function of pH (Fig. 3) (Blum and Laaga

1988, Brady and Walther 1989, Chou and Wollast 1985, Hellmann 1994, Welch and

98
GEOMICROBIOLOGY

ilma 1993, 1996). Acidic or alaline compounds produced by microbial metabolic

rocesses may mediate silcate weathering by changing solution pH. At the pH of most
ltural environments, 5-8, experimentaly detennned mieral dissolution rates ar lowest

id essentially independent of pH (Brady and Walther 1989, Chou and Wollast 1985

Barker, Welch, Banfield: Biochemical Weathering of Silcates

399

Because carbonic acid is a wea acid, microbial respiration may not signficantly impac

minera weathering. However, lithotrophic microorganisms also produce other strong

inorganc acids, primarly sulfurc and nitrc from oxidation of reduced sulfur and nitrogen

and can cause severe but localize pH changes and increased weathering of minerals

sediment microenvironments), or due to anthopogenic activity (e.g. wells, mining, etc.)

between oxygenated and anoxic environments (e.g. in biofims, microbial mats, soils or

compounds. Reactions involving reduced sulfur compounds generaly occur at interfaces

ites increae by a factor of aH+n where n is the fractional dependence of mieral

felch and uilman 1993, 1996). As acidity increases, below pH 5, mineral dissolutio~

,ssolution rate on proton activity and is related to proton adsorption on the minera surface

(Berthelin 1983. Sand and Bock 1991; Nordstrom and Southam, this volume). Nitrifying
bacteria, those that oxidize amonia to nitrate, have been implicated in leahing of cations

.7

.ai

-9

..

6 B
pH

10

1979).

oII
H-C-OH

i.

H-C-C-OH
i

H 0
Acetate

H-C-C-C-Oli
i.

Citrate

",-Ketoglutarate

Malate

Succinate

Ii Ii

Iii iIiJl0

Propionate

Formate

..

o 0

HO-C-C-OH

Hl iOHo
II

H-C-C-C-OH

l; 9 t?

H H

Lactate

H-C-C-C-Oli

Aconilale

fi

If f l Ii
H o-c-c-c-c-c-o
Ii

H o-c-c-c-c-o Ii

Iii Ii, Ii,

o Ii Ii 0 0

i i I U

Ii Ii OHO

H Ii

Ii o-c-c-c-c-o Ii

oII Hl: HI ll
0

Pyruvate

Oxalate

from rocks and soils by acidolysis and ion exchange (Berthelin et al. 1985, Lebedeva et aL

3lum and Laaga 1988). Similarly, in basic solution above pH 8-9, mineral dissolution
,tes increase by a factor proportonal to 8.H.m. where m is related to the adsorption of

N.e

.,
'"

.$

-S

l:

'"

.. .10

.11
4

ydroxyl ions (Blum and Lasaga 1988. Brady and Walther 1(89). The pH dependence
of
neral dissolution varies with mineral composition, oxidation and coordination statef
,ns at the mineral surface, and zero point of charge.

gure 3. Si releae rate from

.dspar as a function of pH in
lutions. Organic acids enhance

Jrganic (.) and organic (e)

dspar dissolution from acidic to

ulr pH (data from Welch 1991).

The combination of respired CO2 with water to form carbonic acid constitutes the most

Ii. 0"

H--C-OH

H 0

C-C-QH

II ?

i II
H--C-Oli

H-C-C-O H

1 991). The simplified form of these compounds is ilustrated in Figure 4. As is the case

(Bertelin 1983, Johnston and Vesta 1993, McMahon and Chapelle 1991, Palmer et aL

oxalate, formate, propionate, lactate, pyruvate, citrate, succinate and a-ketoglutaate

main component in biogeochemical weathering of silcate minerals. Microorganisms

produce and excrete a varety of low molecular weight organic ligands including acetate,

Low molecular weight organic acids, in paricular oxalic, ar most often cited as the

Organic adds

Figure 4. Structures of common organic compounds produced by microorganisms.

Ii

1 ?

I ?

HO-C-C-O Ii

isic biochemical species thought to aclerate mineral weathering. Carbonic acid is a

latvely weak inorganic species but can afect silicate mieral weathering rates

ith atmospheric pCOz ( 350 ppm) is approximately 5.7. However, dissolution rates of

H--C-OH
i

teracting with mineral surfaces. The pH of low ionic strength solutions in equilibrium

ost silcate minerals are pH independent at crcumneutral pH, so carbonic acid in rain or
rface run off may have little enhancement effect over hydrolysis reactions. Respiration by
ant roots and microbial degradaon of organic matter can elevat carbonic acid

,ncentration in soils, sediments, and groundwater by several orders of magnitude,

esumably leading to an increase in minera weathering rates (Chapelle et aL. 1987,

:hwarman and Yolk 1989, 1991). Acidity in natural waters rarely decreases below pH
5 due to carbonic acid, however. This is approximately the pH where minera dissolution

id production by organisms in soils and sediments wil depend on how sensitive

tes star to increase with acidity (Drever 1(94), and increased weathering due to caronic
actions are to changes in pH in this range (-4.5 to 6). Drever (1994) estimates that it will
at most a factor of 3. At very high tota CO2 concentrations and high ionic strengths,
icate mineral dissolution may be inhibited as carbonate complexes with meta sites on the

ineral surface, or insoluble carbonates precipitate on mineral surfaces, limiting hydrolysis

actions (Ferris et al. 1994, Wagelius and Walther

.00
GEOMICROBlOWGY

vith any acid species, numerous studies have demonstrated increased minera dissolution

ares in vitro. Many of these ligands do occur in soils, sediment pore water, and aquifers
1 sufficient concentratons to signficantly impact silcate minera weathering. Several tens
) hundreds of micromolar concentrations of oxalate, formate, citrate, malate, and aconitate
in

Barker, Welch, Banfield: Biochemical Weathering of Silcates

401

996). Silca releas rates in 1 mM oxalate solutions were 2 to 5 times higher in acid (pH

cOre dramatic. At near neutral pH, AI release from plagioclas feldspars was 10 to i 00

) and 2 to 15 times higher at near neutr pH. The effect of oxalate on AI release is even

mes greater than in the inorganic controls. However, oxalate also enhanced the dissolution

ra of quarz, olivine, and a cemented sndstone (Bennett et al. 1988, Grandstaff 1986,

Johnston and Vestal, 1993) suggesting that it can bind to Si, Fe, and Mg sites as welL. This

ave ben found in rhizosphere soils (Fox and Comerford 1990, Grierson 1992) and

Of less soluble ions (pnmarly AI and Fe) from minerals at the pH of natural waters

solutions compared to inorganic controls (Johnston and Vestal 1993). This change in

llman 1992, 1993). However, in inorganic solutions at neutral pH, Si is preferentially

moved, leaving an aluminum nch residual phase (Manley and Evans 1986, Stilings et aL
996, Welch and Ullman 1993). Therefore, oxalate production by microorganisms should
referentially solubilze AI from minerals due to both its acidity and complexing abilty.
!ccasionally, net calcium release to oxalate solutions were less than the stoichiometrc ratio
in the mineral phase, presumably due to the formation of insoluble calcium oxalate phases
(Welch 1991). Sandstone leaching experiments showed a decrease in Ca releae in oxalate

eldspar, leaving a residual solid phase ennched in Si (Mast and Drever 1987, Welch and

ature of dissolution products. For example, oxalate increased AI release to solution from

In addition to enhancing the overal mineral dissolution rate, oxalate can also affect the

(Antwei1er and Drever 1983, Stilings et al. 1996, Welch and Ullman 1993).

implies that ligand promoted dissolution is parcularly importt for increasing releae rates

~sser amounts in non-rhizosphere soils. Organc acid concentrations in oxic

ncontamnated groundwater ar generally very low, on the order of a few to few tens
ut migrate from organic nch or reducing zones (McMahon and Chapelle i 991, Thurman

1icromolar concentration. These organic acids ar often not produced in situ by microbes

985). Organic acids, pnmarly fermentation products, have been measured in shallow

noxic groundwater with concentrations ranging from a few to few tens micromolar
Welch, unpub) though much higher concentrations, micromolar to millmolar, have ben
~ported in marine sediments (Peltzer and Bada 1981, Sansone 1986).

icreae mineral weathenng by proton attk at the mineral surface. Ligands ca attk

Naturally-occurrng organic ligands increase dissolution rates and afect the dissolution
toicluometry of rocks and minerals. Although most organic acids are weak, they can

iinerals directly by complexing with ions at the surface, weakening meta-oxygen bonds,
od catyzing dissolution reactions. Ligands also indirectly afect rates, by complexiiig

weather in organic nch (soils, lichens) verses organic poor (groundwater) environments.

iith ions in solution, lowering solution saturation state. The enhancement of minera
isso1ution by organic acids increases with organic acid concentration (Stilings et al. 1996,
'andevivere et al. 1994, Welch and tJ1man 1992) or increasing reactive sites at the mineral

Varadachar et al. (1994) used SEM and light microscopy to examne silicate minerals

dissolution stoichiometry should result in different secondar phases fonnng as minerals

Jrface (Huang and Kiang 1972, Manley and Evans 1986. Stilings et aL. 1996, Welch and

ruman 1993, 1996). Bidentate ligands, such as oxalate and succinate, increase overall
iineral dissolution rate much more than monodentate ligands such as acetate. Of all these

(olivine, epidote, tourmaline, hornblende, biotite, ncrocline) reacted with oxalic acid.
Minerals containing high concentrations of Al+3 and Fe+3 were extensively etched,

As always, extreme caution in applying laboratory denved data to natura environments

be used. In the cas of oxalates, however, an insoluble crystalline oxalate forms by
combination with appropriate cations. Many fungi are known to synthesize oxalic acid and

tched with euhedral pnsmatc etch pits while garets dissolved in inorganic solutions were
as extensively etched and had more irregular pit morphologies (Hansley 1987).

Heeted the morphology of minera etching. Garets dissolved in oxalate were deeply

ther unidentified amorphous and crystalline phases were also observed. Oxlate also

aterial, presumably from precipitation of insoluble divalent-meta oxalate complexes.

resumably due to the formation of soluble metal-oxalate complexes. However, minerals

ith divalent catons (Ca+2, Mg+2, Fe+2) tended to have these ions in the residual solid

:ids, acetate and oxalate are the most abundat organic acids in natural systems (Fisher
987, Kawamura and Nissenbaum 1992, Marens 1990, Sansone 1986, Sansone and
arens 1982, Surda et al. 1984). Acetate can be produced by both abiotic and biologicl

rocesses. Concentrations greater than 10,00 ppm have been measured in

asins and acetate has been deteted at temperatures up to 200T (Kharaka et al.
urdam et al. 1984). Expenmental minera dissolution studies have demonstrated
;etae enhances silcate mineral dissolution and may be importt in mobilzing ions in
Ufield formations waters. Acetate, however, is much less effective than oxalate in
1hancing mineral weathering.

Oxalate. High concentrations of oxalate have also been measured in natural systems

:;ox and Comerford 1990, Johnston and Vesta 1993, Kawamura and Nissenbaum 1992,

!acGowan and Surdam 1988, Peltzer and BOOa 1981). It is produced and released by a

Jories 1984) provides a relatively unambiguous correlation between laboratory and field

their hyphae are frequently found encrusted with crystalline oxalates. Calcium oxalates"also
accumulate to high levels in some forest soils (Graustein et aL 1977). Additionally the
presence of insoluble oxalates whose chemistry reflects that of the substrtum (Wilson and

)ncentrations are high enough to precipitate oxalate salts (Ascaso et aL. 1990, Graustein et

mety of plants and microorganisms, paricularly fungi. In some microenvironments

1993). Because oxalate is one of the most abundant ligands

1977, Johnston and Vestal

ichen substances are often cite as dissolution agents (Wiliams and Rudolph 1974).

Each lichen association produces a unique and relatively diagnostic suite of compounds
called lichen acids or lichen substances (Huneck and Yoshimura 1996). As a genera rule,
neither isolated symbiont produces lichen acids, (Jones 1988) which apparently result from
pecific interactions between mycobiont and phycobiont. In lichen weathering of minerals,

Lichen acids

ar parcularly compellng evidence of the involvement of oxalic acid in mineral weathering

in natural sy stems.

sulfide bearing rocks, and by Wilson et al. (1980) of glushkinite (a rar manganese oxalate)

studies. Report by Purvis (1984) of copper oxalates within lichens colonizing copper

~tecte in solutions interacting with mineral surfaces, many laboratory studies have
icused on oxalate promoted mineral weathenng.

Most laboratory mineral weathering studies using oxalate have demonstrated a

gnificant increae in the relea~e of major ions from rocks and minerals compared to
)ntrols. Manley and Evans (1986), Huang and Kiang (1970) Huang and Keller (1972)
ieasured a one to two order of magnitude increase in releas of ions from minerls

Jmpared to controls in batch dissolution expenments using high conccntrations of oxalate.

.owever, they attbute enhanced dissolution to the acidity of oxalate, and not to ligand
romoted dissolution. More detaled mineral dissolution experiments showed that oxaate
ihances dissolution of the feldspar framework compard to inorganic controls over a
mge of pH (Bevan and Savage 1989, Stillngs et al. 1996, Welch and Ullman 1993,

402
GEOMICROBIOWGY

shown to increase mineral dissolution rates in laboratory experiments (Ascaso and Galvan

Despite limited solubilty in water, saturated solutions of lichen substances have ben
1976, Iskandar and Syers 1972) via chelation. Nonetheless, reports of naturally occurrng
lichen acid-metal complexes are rare. Purvis et a1. (1987) reported copper-norstictic acid
and copper-psoromc acid (Purvis et al. 1990) complexes in oddly pigmented green lichens

growing on cupriferous rocks. Usnc acid did not form a copper complex. One species of
lichen growing on these cupriferous rocks contaned norstictic acid that was not complexed
with copper. Thus, Purvis et al. (1990) concluded that copper only complexed with lichen

substances when their locations withn the thallus coincidentally overlapped.

Barker, Welch, Banfield: Biochemical Weathering

403

diffusion pathways as water potential decrases (Chenu and Roberson 1996), acidic
functional groups (chelation and ligand formation) and by acting as nucleation sites for
authigenic mineral formation (Barker and Banfield 1996, Barker and Hurst 1992, Fortrin et
al., this volume; Urrtia and Beveridge 1993, 1994).

Schwarman and Vo1k (1991) emphasized the importce of soil binding by

microorganisms as a major factor in increasd mineral weathering by microorganisms.

Polysacchardes are widely recognized as the chief organic component involved in sediment

volution of mechanisms with which to guard against dehydration. From a biological point
fview, the large investment of a microorganism in constructing a capsule, sheath or slime
yer is explained as creation of a controlled microenvironment, as well as a defense against

binding by microorganisms (Dade et al. 1990, Forster and Nichols 1981 a,b). Perhaps the
ost important barier to microbial colonization of terrestral surfaces would have been

redation and desiccation (Ophir and Gumick 1994). From a mineral weathering

Lichen substances are usually concentrated in the upper thallus near the algal
these substaces crystaliz on the upper surface as a pruinose covering. Therefore, a more

phycobiont, not at the mieral interface (Thomson, pers. comm. 1994). In other cases
plausible interpretation for the tre role of lichen substances may be to deter predation

increase th residence time for water to fuel hydrolysis reactions which characterize low

1978). In any case, the lack of reported meta-lichen acid complexes, limited

temperature silcate minera weatering. i~nother contribution EPS make to silcate mineral
eathering is to maintain diffusion pathways as water levels decrease (Chenu and
.oberson 1996). Increased residence times and interconnected diffusion pathways in

perspective, the abilty of these polymers to retan water is especially important as

(Lawrey 1980). Additionally, the lichen may use these compounds to regulat the opacity
of the upper thallus to optize light levels for the phycobiont (Lawrey 1986, Rundel

water and their location in the upper thallus suggest they do not play an importt role in

rficial weathering environments characterized by irregular water supplies would increase

eathering rates from this standpoint alone.

mineral weathering.

Sideropliores

roups, primarly uronic and teichoic acids (caboxylated and phosphorylated

ered minerals show extensively etched surfaces surrounded by EPS (Barker and

bohydrates, respectively), that can react with ions in solution and on surfaces. Naturally

In addition to their antidessication properties, these compounds contain functional

Under conditions of iron limtation, microorganisms produce special iron

ligands caled siderophores which complex with and transport iron to the cell (Stone
WOOs dalton) compounds that have a very high affinity for Fe+3. There are two

Nealson, this volume). Siderophores are soluble, intermediate-molecular-weight (100s.to

ld 1996). Experimental weathering studies with slime fonnng microorganisms and

icrobial EPS showed that the polymers could indeed increase mineral dissolution, though

classes of these compounds, hydroxamates and catecho1s. Both form bidentate

ey were not as effective as the low molecular ligands (Malinovskaya et a1. 1990, Welch

this single species is known to synthesize 50 antigenically distinct adhesion proteins

chanan 1975)! Is there any reason not to suspect similar complexity and specificity in

to specific surface recognition and attachment mechanisms. For example, the

genicity of Neisseria gonnorrheae, is known to be directly related to its abilty to
thesize proteinaceous adhesive appendages (Brinton et al. 1978). Mutated strains
pab1e of manufacturing these proteins lose their abilty to adhere to cell surfaces in
ans and their ability to cause venerea disease. The astonishing aspect of this story is

ature on microbial interaction with surfaces. Microbial pathogenicity is often intrcately

The involvement of microorganisms in human disease has generated an extensive

'4), thereby moderating mineral precipitation reactions.

acellular polymers can also serve as nucleation sites for secondar mineral phases
er and Banfield 1996, Konhauser and Ferrs 1996, Urrtia and Beveridge 1993,

ve been due to the precipitation of a secondar phase because microbial cell surfaces and

available for further reaction. The apparent inhibition of silcate mineral dissolution could

nds are irreversibly binding to reactive sites on the surface, making them

d Vandevivere 1994). Malinovskaya et a1. (1990) determined that mixtures of polymers

low molecular weight ligands had a synergistic effect on weathering. In a similar study
wever, mineral dissolution was inhibited in solutions with microbial EPS compard to
mic acids alone (Welch and Vandevivere 1994), indicating the higher molecular weight

1995, 1996; Holman and Casey, 1996). Hydroxamate siderophores produced by

ar

chelates with Fe+3 with stabilty constants on the order of 1030 to 1040 (Hersman et a1.
and fungi significantly enhanced dissolution of iron hydroxides and Fe+3 containing

minerals (Hersman et al. 1995, Wateau and BerteHn 1994). Catechols forms very
bonds with mineral and meta surfaces (Kummert and Stumm 1980) and increase
dissolution rate of silcate mineras in vitro (Welch and Ullman 1996).
containing catechoJs and hydroxamates may bind with other major ions in
especially A1+3, acclerating mineral dissolution (Ochs et al. 1993, Watteu and
1994).

Polysaccharides
Bacteria and other microorganisms synthesize extrcellular polymeric layers which

thought to be a complex mixture composed primarly of extracellular polysacchardes

mineral weatherig studies. In the initial stages of attahment, microorganisms are. only

(EPS). Despite numerous studies demonstrating bacteria commonly atthed to surfaces in

natural environments (see Little et aI., this volume), the mechanisms and biochemistr
involved in microbial attahment to surfaces has received comparatively little attention in

weaky adsorbed to the surface substrate (reversibly attached). Bacteria seem to "sense"

when they ar in contact with a surface, and with time produce extracellular
polysaccharides (EPS) and other compounds which enable them to irreversibly atthto

surfaces (see microgaph on cover of this volume) (Fletcher and Floodgate 1973). BPS

Vandevivere and Kirchman 1993).

adhesive mechanisms between mineral surfaces and microorganisms? The dental

atur also contains a wealth of literature concerning microbial atthment and cavity

production is greater for attched verses free-living bacteria (Davies et al. 1993,
Polysaccharides impact mineral weatering in five ways: binding soil (see sectionory
soil stabilization), antidesicant (increasing the residence time of water), maintaning

404
GEOMICROBlOWGY

Figure 5. P-type sex pilus (P) of Escneriscnia coli (B) adsorbed onto the basal surface of kaolinite
Arow indicates metal deposition direction. Propane jet cryofixed. frze-etch Pt-C replica, bright
transflssion electron flcrograph (Barker i 988).
While several excellent reports detail the involvement of proteins in mineral nucleation

(Schultze-Lam et aL. 1992, 1994, 1996), almost nothing is known regarding the role of

these biological molecules in silicate mineral weathering. Microbial cell surfaces ar

comprised of approximately 40% protein, and these compounds should be able form
complexes with ions very similar to ones formed by polysacchardes (Brock et al. i 994,

Hughes and Poole 1989). Amno acids and polypeptides are known to adhere strongly to
silcate mineral surfaces (Fig. 5) (Barker 1988, Barker and Hurst 1993, Dashman and
Stotzky 1984). Microorganisms also produce enzymes that ar speifc for binding meta

ions or that require meta ions as par of Ll-er structure, however its not known if thes
enzymes playa significant role in mineral weathering. It is well known that organisms

as lichens and fungi grow on durable, organic materials (e.g. polysaccharides, c

cellulase) that may have crystaline structures with periodicities not dissimilar to
found in silcate minerals (e.g. Chanzy et al. 1996). Microorganisms produce enz
(e.g. chitinase and cellulase, often bound to the cell wall) speificaly to degrade th
substrates. Do microorganisms living on rocks (e.g. lichens) or in soils produce enzy
(or other high molecular weight molecules) that function in ways arialogous to chitinase

cellulase ("nneralases"?) to break down minerals that they grow on in order to

elements required for metabolism or structural purposes? Speculation about the existence
such "mineraIases" has not lead to a sustained research effort, but that is only a matter

Barker, Welch, Banfield: Biochemical Weathering of Silcates

405

time. Now that advanced molecular techniques such as two dimensional gel electrophoresis

have been developed and scientists trained in molecular techniques are turning their
atention to geomicrobio10gy, a level of specificity undramed of today in the ancient

relationship between microorganisms and mineral surfaces may well emerge.

Microorganisms can afect minera reactions by serving as a sink for elements releaed

by weathering. Mineral dissolution rates are a function of solution saturation state. At far
from equilbrium conditions, mineral weathering rates are independent of solution
satration state, then as solution approaches equilbrium with respet to the dissolving
phase, rates derease. Several biotic weathering studies have demonstrated that plant roots,
fungi and bacteria dramatcaly increased K, Fe, Mg, and AI releae from micas, and that

these organisms served as a paral sink for these elements (Hinsinger et al. 1993,

Rinsinger and Jailard 1993, Leyval et al. 1990, Mojal1ali and Wee 1978). These

organisms also increase the transformation of biotite to vermculite by takng up K+ that

as released from the biotite structure (Hinsinger and Jaillaird 1993). However, none of

e biotic mineral weathering studies have demonstrated unequivocally that nutrent

id and ligand production, could also account for the observed changes in mineral

dsorption by microorganisms increases weatering rates, beause other factors, such as

eathering. Abiotic weathering experiments using micas and ion exchange resins have
monstrated that weathering rates increased substantially when ions were removed from
solution (Lin and Clemency 1981).

MINERAL WEATHERING STUDIES

Silca is an essential nutrent for many organisms. Some microorganisms, such as

iatoms (Gordon and Drum 1994), radolarans, and frustules actively precipitate intrcate

"iceous tests, even when bulk solutions ar extremely undersaturated with respect to

orphous silica (de Vrind-de Jong and de Vrind, this volume; Konhauser et aL. 1992).
'crobial cell walls and EPS also serve as a substrate for amorphous silca precipitation

rtin et aI., this volume; Jones et al. 1997, Urritia and Beveridge 1993). Many 1gher
irganisms, such as plants and sponges, form siliceous support strctures (phytoliths and
icules, Alexandr et al. 1997, Bavestrello et al. 1995). Trae amounts of silca are also

quired for other strctual organic compounds. Since silca is an essential nutrient

uired by many organisms it seems plausible that microbes have developed mechanisms
actively extract silca from silicate minerals.

Quar, a framework silcate with the composition Si2 (see detals in Banfield and

amers, this volume), is extremely resistant to chemical weathering. Unlike most other

licate minerals, quar dissolution is unaffected by acidity except at extrmely low pH,

5S than 2 (Brady and Walther 1990). Dissolution rates and quar solubility are enhance

nds. Although quar dissolution is unaffected by production of inorganic acids, both

bstantially as pH increases above approximately pH 8 due to deprotonation of Si-O-H

re was a strong corrlation between DOC and dissolved Si, indicating that microbial

and experimenta data demonstrate that quar is susceptible to organic ligand attck.
'efore, microbial production of organic ligands potentially ca moderate geochemical
ions involving silca. Hallbauer and Jahns (1977) reported that fungal hyphae etched
ar grains as well as other silicate minerals. While the mechanism for this atk was
known, presumably it was due in par to the production of low molecular weight organic
ids. In petroleum contamnated aquifers, quar sand was extensively etched compared to
ains outside the contamnated zone (Bennett and Siegal 1987, McMahon et al. 1995).

06

GEOMICROBlOWGY

Barker, Welch, Banfield: Biochemical Weathering of Silcates

407

1974, Kutuova 1969, Webley et aL 1963). Microorganisms can also produce alaline

2000

1500

50

1969).

:i

:: 1000

500

4G

compounds and increae feldspar weathenng by hydroxyl promoted dissolution (Kutozova

~gradation of oil and production of organic ligands catalyzed dissolution. Quar dissolved

6. Si (e) and AI (I~)

time (days)

20 30

ren though solutions were nearly saturated with respect to amorphous silca (Bennett and

from feldspar in solutions

1 II

dgel1987).
In abiotic laboratory experiments, quar dissolution was enhanced by organic ligands
)mpared to inorganic controls. The effect was less pronounced than that observed in the
eld, indicating high organic content in bulk solution is not solely responsible for the Si
,leaed from quar (Bennett et al. 1988, Bennett and Siege! 1987). Microorganisms in

einen 1974).

ilture were also able to increae dissolution of quar and biogenic or anlOrphous s1ca by
toducing organic ligands or alkaline compounds (Avakan et aL 1984, Lauwers ard
Higher organisms also have the abilty to eth quar (Bavestrello et aL. 1995). The
lemospongiae have slceous skeletons usually composed of opaline spicules, although

m.formis, forms its skeleton from a wide rage of foreign paricles. Bavestrello et aL

)me species incorporate other allocthonous parcles as welL. One species, Chondrosia

1995) examined silcate minerals from the ectosome of these sponges using SEM. Mostof

(A.). Bacteria gratly en-

bacteria and Si release in a

S i and AI releae frm

the

ie silcate minerals and opaline silcate parcles appeared unaltere by the sponge, though
ctosomes of sponges the quar grain size decreased and suifaces were extensively etched

rystallne quar was highly etched. When quar and opaline silca were placed in

Banfield, previoiisly unpublished

by producing organic an
inorganic acids (Welch, Barker an
data).

iithin a matter of days, while the opaline silica appeared unaltered. The sponges

gnificantly increased dissolved Si released to solution from quar sand compared to

1Volved in producing collagen at the site of quar dissolution, and quar

roduction of organic ligands resulted in feldspar suifaces depleted in cations and enriched

stoichiometnc weathering characterized mineral reactions at the lichen-minera inteifac.

The question of stoichiometr is central to understanding the effect of biological

ocesses on silcate mineral weathering reactions. Several studies concluded that

1979, Welch 1991).

r il11aboratory studies simulating natural conditions (e.g. Jones et aL 1980, Holdren and

weathered in different environments (Aldahan and Morad 1987, Berner and Holdren 1979)

1980, Wilson et al. 1980, 1981). Similar etch features were observed on feldspars

feldspars in natural environments. Much of this work has focused on minera suifaces
under lichens. SEM examinations of feldspar suifaces under lichens showed highly etched
'heral suifaces. Formation of etch pits appear to be crystalographically controlled
ause the pits were euhedral and often occurred in linea pattrns, indication that they
ere fornng along twin planes, exsolution lamellae or other crystal defects. The etching
attern depended on the type of feldspar and the mineral fac (AdanlO et al. 1993, Jones et

much lower and bulk solution pH ranges from 5 to 9. However, there is field basd
evidence that microorganisms and microbial metablites ar importt in weathenng of

more realistic field conditions where microbial cell numbers and nutrent concentrations are

As noted above, it is diffcult to extrapolate results of these types of experiments to

parcularly important in enhancing feldspar weathering at near neutral pH.

AI releas to solution (Welch 1996, Welch and Ullma 1995). Therefore, both biotic and
abiotic experiments indicate that microbial production of organic ligands might be

ofSi releae was correlated with production of complexing organic acids which catayze

compard to controls without a significant change in bulk solution pH. This enhancement

subsuiface bacteria produced organic ligands and increased S release from feldspar

011 mineral dissolution. Vandevivere et aL. (1994) demonstrated that several strains of

In most studies of microbial weathering of feldspars, it is very diffcult to decouple the

synergistic effects of production of complexing organic ligands and decreasing solution

biotic control. The authors implicated ascorbic acid because it is the

olutions of ascorbate. However, ascorbic acid should have acted on other silcate minerals
s well, parcularly AI- and Fe-silicates. Natural saiuples of these minerals found in

ponge ectosomes had well shaped crystalline features as opposed to the spongy
~xture on quar suifaces. It is likely that additional mechanisms may have acted in
vith ascorbic acid to produce the observed extensive quarz dissolution.

i'eldspars
Feldspars are the most abundant aluminosilcate mineral at the Ear's surface.
trcture is described by Banfield and Hamers (this volume). Feldspars are more

o microbial atack than quar because they contain ions that react strongly with
roduced compounds. Dissolution and weathering reactions involving feldspars

ieutralizing acid rain. Over geologic time scales, weathering of Ca-silcates

(udied extensively in the last few decades because weathering of mlnerals is

)Iagioclase) regulates atmospheric CO2 concentrtion. Weathering of alkali feldspars

'e1eases K+, a major nutrient necessar for plant growth. A general feldspar

'eaction can be describe as dissolution of the prmar feldspar mlneral releasing

iolution, fonowed by precipitaion of a seconda clay phase. (For an excellent
'eldspar dissolution studies see Blum and Stilings (1995)).

Laboratory studies demonstrate that microorganisms substantially enhance

:1issolution rates by producing acids (Fig. 6). Vandevivere et al. (1994) measured a
fold increase in Si release rate from a Ca rich plagioclase in an acid producing
culture compared to an abiotic control. Similarly, Bertelin (1971) meaured a
increase in AI concentraton from a grantic sand reacting in an acid
cultue (pH - 3) compard to an abiotic control. Many other laboratory
nutrent rich solutions) on microbial dissolution of minerals have demonstrated a
enhancement in concentration or release rate of major ions from feldspar.
primarly bacteria and fungi, produced acids (both inorganic and organic) and
bulk solutioii pH (Avakyan et al. 1981, Vandevivere et at 1994, Wiliams and

Barker, Welch, Banfield: Biochemical Weathering of Silcates

409

GEOMICROBlOLOGY

an by soybeas alone. MuscoVte was not affected by biological weathering. The authors

Be1gy (1979) reported the complete removal of K and Ti from biotite in a grantic sand

umented K and Ai depletion from flake edges using an electron microprobe. BerteJin

'Oorganisms in the rhizosphere increed the availabilty of K+ from biotite to Zea

e, white micacous parcles. Bertelin and Leyval (1982) found that symbiotic

a cormunity of bacteria and fungi afer a 22-week perfsion experiment, resulting in

ys, and furer noted that addition of non-symbiotic microorganisms promoted much

08
Si, with amorphous or poorly crystallne material forming at the interfac. In the absence
, organic ligands, surfaces were enriched in AI and secondary phases, primarly clays
ere formed at the lichen mineral interface (Ascaso et al. 1990, Jones et al. 1980). Thes~
Jservations agree with laboratory studies which show an increase in AI release to
lutions with complexing organic ligands or decreased pH (Welch and Ullman 1993
196, Stillngs et al. 1996). It is importnt to remember that these studies of natura

mduced at distace from the lichen thallus, biogeochemica weatering involved complete

own exposure age. In contrast to topotatically oriented smectite and Fe-oxyhydroxides

'rectly compared by Barker and Banfield (1996) in a lichen-colonize syenite boulder of

Biogeohemica and physiochemica weathering of ferrohastingsite amphibole was

ts and denticulations which resembled those seen in ultrasonically cleaned, naturaly

athere soil grains (Berner and Schott 1982), Schott et al. (1981) produced caon
p1ete silca enriched surface layers in iron-free pyroxenes and amphiboles with acid
atments. Banfield and Barker (1994) and Barker and Banfield (1996) found no evidence
rsurface depleted layers in naturally weathered amphiboles.

ve been parially successfuL. While Berner et al. (1979, 1980) were able to produce etch

Effort to reproduce nara weathering conditions for chain silcates in the laboratory

ween the chemistr of the parent amphibole and smectite, indicating very limited
ansport of dissolved constituents.

~stry closely approximated the parnt phas. Studies of naturally weathered coexisting
phiboles (Proust 1985, Banfield and Barker 1994) also demonstred a close correlation

pyroxene initially weathered under lateritic conditions to an amorphous product whose

t always the case (Singh and Gilkes 1993). Nahon and Colin (1982) found that

ectites, topotactic relationships between the primar and secondar phases ar often
und (Eggleton 1975, Banfield et al. 1991, Banfield and Barker 1994), although this is

ctura relationship between the I bea of chain silcates and the T-O-T layer of

field et aL. 1991, Banfield and Barker 1994, Singh and Gilkes 1993). Due to the close

uminous weathering products and the ultimate formation of relict cleavages known as
icroboxworks by a dissolution-reprecipitation mechanism. In the case of amphibole and
xene transfomung to smectite, the reaction is isovolurnetric (Fig. 8) (Colin et al. 1985,

994), although kaolinite (Ve1bel 1989) and tac (Eggleton and Boland 1982) also have
n reported. Velbel (1989) explained the transformation of hornblende to ferrginous and

action proceds along cleavages and grain boundaries to produce a varety of secondar
inerals. Most frequently, smectite, AI and Fe oxides and oxyhydroxides or complicated
ixtures (Fig. 7) of these minerals form (e.g. Banfield et aL 1991, Banfield and Barker

d Hamers, this volume, for strctual details) demonstrate that the cleavage-controlled

Natral and laboratory studies of weathering of pyroxene and amphibole (see Banfield

netration by microorganisms. More recently Leyval and Berthelin (1991) confirmed these
suits by investigating the effects of rhizosphere microorganisms of pine to extract K+
om phlogopite. A far more interesting result was their report of a spatial corelation
:tween rhizosphere microorganisms and aras of highest K depletion. Fritz et aJ. (1994)
umented a similar K+ gradient in soil solutions from pine rhizospheres cormunities.
any field studies, parcularly investigations of the effects of lichens on rock weathering,
ave documented biophysical disaggregation and mineraogical transfoiiation of biotite to
,rmculite and smectite (Barker and Banfield 1996, Wierzchos and Ascaso 1996).

rnkel (1977) attributed observed weathering of biotite in estuarine sands to interlamellar

ore biotite weathering and K uptake, an effect they attbuted to "better soil exploration".

aterial all employed intense digestion of organic materials with boiling hydrogen
~roxide. As noted above, such intense chemical treatments destroy all textual information
id drastically alter the mineralogical component. Barker and Banfield (1996) examned the
tact organc-mineral interfac in a lithobiontc lichen cormunity using HRTEM and found
J evidence of leached layers or silceous relicts on amphibole, feldspar, or biotite.
Bacteria are also importt in increasing feldspar weathering rates. In situ microcosm

udies (Bennett et aL. 1996, Bennett and Hiebert 1992, Hiebert and Bennett 1992) in an
uifer contannated by an oil spil show that feldspar and quar weathering was increased
e size and shape of bacteria. The authors hypothesized atthed bacteria created a micro-

hen bacteria colonizd mineral surfaces. Many etch pits on mineral surfaces approximated

action zone where organic acids and other metabolites were concentrated at th minera
irface, locally increasing the mineral dissolution rate. Mcrobial colonization and extent of

ching depended on feldspar composition (Bennett et al. 1996). Two plagioclase

;ldspars, albite and oligoclase, were sparsely colonized by bacteria and only oligoclase
)peed to be etched by the colonies. Two alali feldspars, microcline and anorthoclas,

J.d much higher surface colonization and were more deeply weathered. The authors
fPothesized that bacteria were potassium limited, and were attking the more potassiumen feldspars preferentially. Estimates of weathering rates base.d on Si mass balance along
flow path and Si releas from the mineral surface due to microbial etching shows that

~arly all the weathering can be attrbuted to the bacteria. Furter experimentation is needed
determne the role that irregularties in crystal structures such as dislocations and crysta
rain in domain boundaries play in microbe-mineral interactions (HocheJJa and Banfield

195, Lee and Parson 1995).

Beas
Micas are layer silcates that commonly contain K as the interlayer cation (see Banfield

id Hamers, this volume, for structural details). Bioavailability of inorganic nutrients, such
; K+, to plants long has ben of interest to soil and plant scientists. Biogeochemica

otite as a sole K+ source, converted biotite to vemuculite in a period of one year.

eathering of micas, in paricular the biotite to vermculite transformation, has received a

-eat deal of attention over the year. Mortland et al. (1956) demonstrated that wheat, given
pyridakis et aJ. (1967) confirmed the rapid conversion of biotite to vermculite and also
:ported epita.xial crystallization of kaolinite overgrowths. While neither of these studies
ientioned rhizosphere microorganisms, no paricular precautions against microbial growth
'e evident in the experimental designs. Weed et aL (1969) documented the abilty of soil
ingi to concentrate K+ when given biotite, ph10gopite and muscovite as a sole K+ source,

:sulting in the production of vermculite. Whle bioavailabilty of K+ varied among

fferent micas (biotite;: phlogopite ;: muscovite), biotite functioned as well as soluble salt

1d K+. While they suggested a possible Na+ ion exchange mechanism, they were carful

eCl) as a source of K+. The authors noted a positive correlation between levels of Na+

educed fungal metabolism and organic acid production is an altemative explanation.

) note that a portion of the experiment took place under reduced sucrose conditions.

10jallali and Weed (1979) speifically investigate the contribution of a soybear

\zosphere cormunity to mica weathering and found increaed production

iterstratified biotite/vermculite and phlogopite/vermculite by rhizosphere microorganism

..o

~
~
Q
()

8
ci
~

Figure 7. Alteration assemblage composed of smectite (S) and nanocrystaHinc goethite (0) which remains following eomplcte

transformation of coexisting riebeckite and acmite. HRTEM bright field micrograph. Ar'ion milled sample. (Barker alid Banfield,
previoiisly unpublished image).

tt
.~

0'

P'

tt

::
(!

P.

tt
~
'"
;:

2
;;
r.

Figure 8. lsovoluinetrie transformation of amphibole to smectite. HRTEM bright field micrograph, Ar ion milled sample. (Banfield
and Barker 1994).

.t
I,.

12
GEOMICROBlOWGY

lssolution and reprecipitation of a complex mixture of non-topotactically oriented smectite

id Fe-oxyhydroxides bound by extracellular polymers (Fig. 9).

BIOGEOCHEMICAL WEATHERING OVER TIME

Conditions on Ea have changed substantially in the last 4.6 Ga, ostensibly from a
~ry hot, high pressure CO2 rich atmosphere to the hospitale climate we know today.
vidence exists, albeit controversial, that biological processes have operated throughout
iost of the Ea's history, even in the most extreme conditions. One major factor afecting
ie Ear's climate is the concentration of COz in the atmosphere. Over geologic time scales

.1OS years) the major sink of atmospheric COz is weathering of Ca-Mg silcates and
ibsequent precipitation of Ca-Mg carbonates (Berner et al. 1983, Yolk 1987, Walkeret at

COz + 2HzO + CaAlzSiiOs =; AliSizOs(OH)4 + CaC03

;l81). The overall reaction can be described by (Berner 1991):

At higher temperatures (due to higher atmospheric CO2), mineral dissolution rate

icrease, leading to an increase in the flux of Ca+z and Mg+z to solution and precipitation of

Barker, Welch, Banfield: Biochemical Weathering of Silcates

413

'~

" .'"
,.

-0 g

is i:Q"

i;

.,
~-;

.g
';i:

~;;
'"

.c'" .c"
x_"
o
tt ::,,
ii

12 j

~.g
.. u

6i:.
~

imperatures. The magnitude of this negative feedback between weathering and clima
~,pends on the temperatu dependence (or apparent activation energy) of the silicate

' i:

rrbonat minerals. This in turn lowered atmospheric COz concentration and global

'eathering reaction.

'- :;

;- )( c:
..
0 ::

:: ro::
on.t O.

t 8:

-:: '".c

e\ . 1

0..=~

i: '" bi

~ E )

--:0 .

.c ~

.: ~
lL~
0.P.
"'~

.c ..

.c
_ '"
0

~t
~r.
~'"
",00

&i

ti 8

i:::

'" .-

.~

S .d
" 0.
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~

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80

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.. .-i:
",-"

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~ ~

Two early geochemical models, BLAG (Berner et al. 1983) and WHAK (Walker et at
981) atmpted to model pCOi and temperature over time by considering various abiotic
eological and geochemical processes. Neither model considered the effects of biological

rocesses on silicat weathering. More recent models by Schwarman and coauthors

khwarman and Yolk 1989, 1991; Schwarman et a!. 1993, Schwarzman 1995,
chwarman and Shore 1996) integrate geomicrobiological parameters in an atempt to

uantify the biological acleration of silicate minera weathering rates, the subsequent
icrease in removal of CO2 from the atmosphere, and resultat lower temperatures.

Biotic enhancement of weathering should change with temperare and pC02. More
nporttly, biological accleraon of minera weathering should progress as life evolved

)mplex metazoans. If the biotic enhancement of silicate weathering is substantial,

ad colonized the Ear's surfac, from the earliest prokarotes, to eukarotes to the more

rganisms can afect the feedback between pC02, temperature and mineral weathering,

iereby moderating the Ear's climate (Schwarman and Yolk 1989, 1991; Schwarman
al. 1993, Schwartzman 1995, Schwarman and Shore 1996).
Biogeochemical weatering models of Schwarman and coauthors asume that ealy
ar atmosphere was a ::100.C pressure cooker with high pC02 and low 02' The

~mperature of Arhea Earh formed a major obstacle limiting biological evolution beause
iore complex life forms (those with mitochondria) could not exist above 60'C

khwarman et aL 1993). First evidence of life occurs at 3.8 Ga (Mojzsis et al. 1996).

nese organisms might have been thermophilc bacteria and Arhae which colonized the

:ar's surface and enhanced weathering rates, thereby cooling Ear's surface.
:yanobacteria are thought to have first appeared approximately 3.5 Ga when surfac
~mperatures had decreased to less than 70'C. At approximately 2.1 to 2.8 Ga, eukarotes

volved with an upper temperare limit of 50'C. At temperatures ~ 50.C, higher plants

nd animals evolved and colonized the Earh's surface. The evolution of all these
f each new life form lead to increases in the biotic enhancement of weathering and a

rganisms was constrained by the upper temperature limits, and the successive appearance
ecrease in global temperatures.

n4
GEOMICROBlOWGY

. In attempting to eval~ate the importance of biogeochemical weathering over geologic

me, we must of necessity attempt to apply modem analogs, for example, weathering of
ninerals in the rhizosphere as a model of continental weathering since the evolution of
iascular plants, weathering of rock surfaces under lichen communities as a model of biotic
veathering by cryptogamic organisms, and even lthotrophic bacteria and Archaea that live

Barker, Welch, Banfield: Biochemical Weathering of Silcates

415

(1992) however, found no noticeable enhancement of weathering by the lichen

Stereocaulon vulcani, attributing Jackson and Keller's (1970) observations to trapping of

aeolian debris by lichen thaltL This spawned sharp debate in the literature between Jackson,

higher plants is much greater than that of the S. vulcani. In a more extensive survey of
these basalts, Brady et al. (1997) examned plagioclase and olivine grains in basalts that

1993, 1996; Schwartzman 1993). Cochran and Berner (996) maintan the contrbution of

Berner, Schwartman, and Drever (Cochran and Berner 1993, Drever 1996, Jackson

had been collected in aras that had a range of precipitation and temperature (elevation) to

n extreme environments (e.g. anoxic, high temperature, high pC02, low pH, Jow nutrent)
is a model for possible biogeochemical reactions between rocks and primitive

cryptogamic crust or lichen-like a~sociation. An interesting side aspect is that for a long
time scientists assumed the Jchen association, whether one considered it a tre symbiosis
(Ahmadjian 1993) or a case of controlled parasitism (Ahmadjian 1995), to be a very ancient

microorganisms have probably coexisted with mineral surfaces for four bilion years and
must have exerted a profound impact on mineral weathering piior to the evolution of
vascular plants. Most of these models assume terrestrial colonization by some sort of

advanced creature capable of isotopic fractionation, it seems reasonable to think

counterpars (Mckay et a1. 1996). Recent isotopic data (Mojzsis 1996) from apatites in the
Isua Fm. in Greenland has been interpreted to show biologically fractionated C isotopes as
far back as 3850 Ma. Allowing for the rarty of rocks older than 3800 Ma, vagares of the
fossil record and a certn period of time required to develop some sort of relatively

the mineralogy and ultrastructure of putative Marian microfossils than their terrestral

interest generated by Marian meteorite ALH84001 is that much more is known concerning

concluded the strcture was not a microfossiL. One interesting result of the intense scientifc

of course no small amount of controversy regarding these putative microfossils (see Buick
1991 for the most rigorously exclusive list of characteristics which must be satisfied to
prove a biogenic origin). By far most of the research performed on Archea microfossils
has been descriptive optical microscopy. Heaey and Veblen (1991) examned Eosphaera
tyleri which had been interpreted as a fossilized cyanobacterium, using TE and

indicates single celled organisms may have existed on the Ear at least 3500 Ma. There is

Knoll et al. 1988, Schopf 1993, Schopf and Packer 1987) and South Afca (Walsh 1992)

Paleontological evidence from organic rich chert in Australia (Awraiiuk et aL. 1983,

enhanced weathering exposes new fresh mineral surfaces for reaction.

grow on H2 + CO2 producing methane and biomass. They speculate that microbially

and water. In these extrmely reducing environments, autotrophic microorganisms

In order to understand possible biogeochemical reactions in the Archean, microbes in

an ecological niche that is as isolated as possible from the rest of the biosphere must be
Stevens and McKinley (1995) examined an assemblage of microorganisms living
deep anoxic aquifers where lithoautotrophs derive metabolic energy from reactions with

enhanced weathering, but also resulted in a decrease in the temperature dependent feeback
between weathering and climate.

Although overall mineral weathering rates under lichens were greater, the temperaturedependent weathering reactions (Ea) are only approximately half the abiotic values. Similar
results were obtained by Welch and Ullman (1996) in laboratory minera weathering
experiments. Bacteria and microbial metabolites enhanced mineral weathering rates but
decreased the apparent activation energy of the reaction. Therefore, early colonization of the
Earth's surface by cryptogamic organisms probably resulted in lower peo2 levels due to

are poiki10hydric and trap water at the mineral surface, increasing time for reaction.

more sensitive to increases in precipitation than bare rock surfaces, beause lichens

were different for colonized verses uncolonized surfaces. Weathering under lichens was

Stereocaulon vulcani increased weathering by a factor of 2 to 18 compared to uncolonized

surfaces. Though weathering increased with temperatue and precipitation, these effects

estimate the biogeochemical feeback between weathering and climate. The lchen

nicroorganisms during Precambria.ri times.

There is little doubt that in modern systems, the presence of soils and asociated biota
ire important in weathering of minerals (Drever 1994, Schwarzman and Volk 1991). The

:olonization of the Ear's surface by vascular plants has been importt in enhancing
nineral weathering rate since the Silurian (Knoll and James 1987). However, the
hese studies often overlook the effect of associated microbes in the rhizosphere soil

nagnitude of this enhancement and the most important factors are stil being debated. The
mhancement in weatering has often been attributed to the activity of higher plants, though
iecause it is diffcult (if not impossible) to decouple the effects of vascular plants and their
l~sociated microorganisms on minera weathering. Not all higher plants have the same

;nhancement effect. Silcate nneral weathering in ecosystems dominated by deciduous

'orests is three to four times greater than in conifer-evergreen dominated systems (Knoll

md James 1987), Therefore, changes in the relative abundances of these ecosystems

;hould affect net global biogeochemical weathering rates and CO2 uptake.

Schwarman and Volk (1989) argue for a present day biotic enhancement of
veathering of two to thee orders of magnitude times the abiotic rate. Contrary to this,
iowever, Drever and Zobrist (1992) estiate a much smaller enhancement in biotic

veathering of granitic rocks, a factor of -7, by comparing fluxes of elements from small
;atchments at different elevations in the Swiss Alps, where vegetation decreases with
;levation, from deciduous forests with 1 meter thck soils to bare rock with no significart
iegetation. Cawley et al. (1969) estimate a factor of -3 increase in weathering of vegetad
iasaltcompared to abiotic rates by comparing alkainity in runoff. Based on laboratory

;xperiments, Drever (1994) argues that the biological production of acids and complexing
irganic ligands in soils should have little effect on iiunera weathering (not more than a
'actor of two). A geochemical model of weathering in soils also indicates that biological
)rocesses (primarily add production) should have little effect, but that physical factors,

Gwiazda and Broecker 1994). The main effect of the biota on mineral weathering in soils

;uch as increaing temperature, should substantially increase mineral weathering rates

s to stabilze soil structure, increase paricle binding and interaction of mineral surfaces

iVith solutions (Drever 1994, Schwartzman and Volk 1991). The rise of vascular plants and
'Ormation of soils may have less of a direct effect on weathering but more of an indirect
~ffect , because this should have dramatically changed regional precipitation compared to
he pre-Silurian landscape (Drever 1994).

Before the advent of vascular plants, the landscape probably was not baren, but more
ikely colonizd by cryptogamc organisms, such as algae, fungi, and bacteria possibly
;imi1ar to modern lichens (Golubic and CampbelJ 1979). In order to estimate the effects .of

Jrimitive cryptogamic organisms on rock weathering, investigators have focused on

~xtreme environments where vascular plants are absent but cryptogams flourish. Another
deal place to investigate rock weathering by cryptogams is Hawaiian lava flows, because
ges are well know and changes in elevation and precipitation yield a range of weathering
'egimes. EarIy work on these basalts by Jackson and Keller (1970) show a thick

",eathering crust formng below the lichen and approximately an order of magnitude
ncrease in weathering rate by lichens compared to bare rock surfaces. Cochran and Berner

16
GEOMICROBIOWGY

airing indeed. Recnt genetic analyses on several lichen associations indicate that many
mgal parners (mycobionts) in lichen associations are not closely related (Gargas et al.
995). The implications are twofold: lichen associatons have arsen multiple times (i.e.

iere are no ancestral forms) and perhaps more importtly for biology in general
arasitism may not be a necessar prendition for symbioses to develop. Another probleni

ir extrapolating modem lichens to Archean landscapes is that of approximately 8500

escribed lichens, only a handful (less than 10) ar cyanolicheiis, a formal association of

i'anobacteria and fungi. One might expet this to be reversed as cyanobacteria are of a

iore ancient lineage than green algae. If an association between fungi (mycobiont) and a
i'anobacteria or green alga (phycobiont) is so easy to form that lichenization arose multiple
mes, perhaps this strengthens the argument for symbioses and cryptogamic crusts arsing
i the Archean. Additionally, the fossil record for lichens is extremely poor (as one might
epet) and the hypothesis by Retalack (1994) that the Ediacaran fauna (600 Ma) represent

)ssil lichens has not ben widely accepted. We only raise these points to urge caution in
Jplying knowledge abut contemporar organisms and biological processes to Arhean
croorganisms. Similar morphologies might well be where the similarty ends.
Actual evidence for terrestral Archea organisms is best described as weak. Whe
idence for Archea paleosols is clear, none are reported to contain any microfossils.

larini (1994) cites the presence of graphite as evidence of a microbial mat associated with
1 Arhean paleosoL Hallbauer (1977) published a remarkable series of observations on
)aI-like seams of carbon (thucolite) which occurs in the Wiwatersrand gold reefs. Ashed
iucolite was examned by a varety of methods and Hal1bauer interprete the structures as
fossl lichen, which he named Thucomyces lichenodes. Additionally, the report
~scribed another fiamentous fungus-like microorganism and evidence for considerable
ological remobilization of Au and U. While Hallbauer (1986) reported that these putative

lamentous mats occurred on ventifacts, he was careful to asribe periodic flooding of

-eviously windswept terrain as the most likely depositional environment. A very rent
iper (Bamicoat et al. 1997) dismisses this report and attbutes thucolite to injection of
:uid pyrobitumen along fractures in a hydrothermal event. Regardless of the nature of the

irliest terrestral microorganisms, arguably the biggest obstale to overcome would have
~n the abilty to withstand dehydration. In this context, perhaps a case could be made that

,e evolutionar progression onto land was preceded by aquatic microorganisms adapted to

omass is found at the intedace between the satuated and unsaturated zone in aquifers

)ilthic niches in the vadose zone of permeable rock units. Even today, the highest
.1adsen and Ghiorse 1993, Rudnick et aJ. 1992). Fluctuatng water tale levels would
the crucible in which terrestral adaptations originated, the most effective method

ive provided as effcient a dehydration selective pressure as an intertdal zone. Regardless

Jlysaccharides (Ophir and Gutnick 1994).

dcroorganisms apparntly use today is to surround themselves with layers of extracellular

SUGGESTIONS FOR FURTHER RESEARCH

In order to understand the impact of organisms and biological processes on low
mperature silicate minera transformations, ion concentrtion data, both in the

iineralogical and organic phases which make up the organism minera intedace ar

~eded. Owing to the enormous mineralogical and biologica complexity, sample

:eparation techniques which preserve the ultrastrctue of the intact organic minera

terface as well as elemental distributions must be applied to these complex

'omineralogical samples. While recent advances in examning intat organic-minera

terfaces with a varety of high resolution electron imaging and spectroscopic techniques
ive contributed to our understading of the complex processes occurrng in these areas,
mdamental questions remain. Microbial exopolysaccharides, hydrous polymers which

Barker, Welch, Banfield: Biochemical Weathering of Silcates

417

contain up to 90% water, are extrmely diffcult to prepare for electron microscopy.

Dehydration arifac render a hydrated gel into a cobwebbed mass. Additionally, organic

solvents used to dehydrte these materials prior to resin embedment effectively elutes
metas from polysacchardes. Different types of polysaccharde can be distinguishen with

the use of selective heavy metal cytochemical staning techniques (Foster 1981). Apar from

establishing the existence, location, and general type of extrellular polysaccharde with

respet to mineral sudaces in rocks and soils, conventional electron microscopy is of

limite usefulness in studying these polymers. For example, what is the elemeiita

fistribution of Fe in extracellular polysacchardes coating the sudace of a weathering

pyroxene within a crustose lichen thallus? As of now no biogeochemical study published to

date has employed cryopreservation, cryoultrancrotomy, or cryomicroscopy (Fig. 10) to

in.vestigate these types of questions. Stelzer and Lehmann (1993) reviewed reent

&.enerate a wealth of chemical data which wil greatly clarfy the intimate interrelationship

developments in cryo-samp1e prepartion and analysis which, if applied creatively, wil

between biological and mineralogical processes. Of course, the sample preparation steps

required to prepare a living community for examnation under vacuum wil always be
subject to interpretational questions and the possibilty of introducing arfacts is a very

Figure 10. Bacteral biofim (DOE SMCC 693) coating an etche plagioclase feldspar grain.

Cryomicroscopy reveas the complicated strctur of extracellular polysacchade in which the cells (B)
reside. High pressure, cryofixed, field emission gun; high resolution-low voltage cryo-scanning electron

micrograph. (Barker, Welch and Banfield, previously unpublished image).

18
GEOMICROBIOLOGY

~rious drawback, even the most sophisticated high pressure

!early, the ideal situation would be to quantitatively observe the
ltural state.

techniques.

community in its

'gure 11. Epifluorescence photomicrograph of bactena (bright spots) on feldspar grains. The bactera
B0428 from the DOE SMCq produce extracellular polysacchardes that "glue" mineral grains togeiler.
Welch, Barker and Banfield, previously unpublished image).

Barker, Welch, Banfield: Biochemical Weathering of Silcates

419

perspectives. This combination of high-resolution structural, compositional, and biological

approaches should provide key insights necssar for understanding natual

geomicrobiological weathering of silcate minerals.

While both laboratory and field studies have demonstrated that microorganisms ca

playa role in mineral weathering, the magnitude of this effect is still unknown. Biological

processes ar extremely importt in miera weathering on rock surfaces and in well

developed soils, but it is difficult to even estimate a net weathering rate, let alone discerning
biotic and abiotic components. Estimates of biological enhancement of weathering in soils

magnitude of biotic enhancement of weathering in different environments. One approach

range from a factor of two to 3 orders of magnitude. Furter work is needed to estiate the

(i.e. as in Bennett et a1. 1996, UUman et at 1996) and then analyze samples comparng

has ben to plac well characterized samples in different environments for several year

sites where organisms ar atthed versus 'bare sites' and attempt to estimate the rate
enhancement due to biological weathering. An alternative approach is to analyze samples
such as building stones, quares, or lava flows whose exposure age is known in order to
quantify field raes of biogeochemical weathering.

CONCLUSION

These ar good times to be a geomicrobiologist! A remarkable confluence of

interdisciplinar interest and techniques promises to exponentially increase our

understading of the timeless dance between the physical and the biological world in which
we live. Consider the following short list of very recent discoveries;

Bacteria have been found living up to 4 kilometers beneath the Ear's surface

A new kingdom, Arhaea is discovered and found to occur commonly (Bames et

(Fredrickson and Onstott 1996).

al. 1994, Zimmer 1995).

Molecular biologists find that perhaps 99.9% of soil microbes are uncultureable and
unknown to science (Amann et aL 1996).

Microorganisms capable of withstanding temperatures in excess of 10aoe form the

basis of chemosynthetic-based food chains around hydrothermal vents at abyssal oc

Of course, we have saved perhaps the most astonishing thing for last-the tantaizing
possibilty that Maran meteorite ALH84001 contains microbial microfossils, the first

depths (Brock et at 1994).

evidence that life exists elsewhere in the universe other than Ea (Mckayet al. 1996).

Confocal scanning laser microscopy (CSLM) and epifluorescence (Fig. 11) offers
mprecedented opportnities to study the strcture and chemistry of geomicrobiological

This single electrifying report has riveted the attention of non-scientists and scientists alike,

ystems in vivo (Rautureau et a1. 1993). Researchers have successfully studied )he

age of geomicrobiology. It falls to us, the new generation of geomicrobiologists, to

wllook back on this time, a time when instrumentation and creative analytcal techniques
converged with crumbling barers between physical and biological sciences, as the golden

and wil stimulate a tsunam of interdisciplinar geomicrobiologcal research. One day we

,1. 1995). By use of the proper fluorescent dyes, one ca study pH gradients on a

tructure of lve microbial biofilms (Wolfaardt et a1. 1994), as well as liquid flow within
hese communities (Stoodley et al. 1994). In addition, CSLM imaging of fluorescent epoxy
ias revealed the thee dimensional pore structure of a porous sandstone aquifer (Fredrichet
;ubmicron scale (Chu et al. 1995, Chu and Montrose 1995 ), as well as monovalent,

integrate knowledge from such diverse aras as the molecular aspets of microbial surface
recognition, data on microbial adhesion and tooth decay from denta literature, and minera

he authors than Paul Ribbe for editorial support. Susan M. Paskewitz and R. Le Penn

ACKNOWLEDGMENTS

dissolution data from the geochemistry literature to produce a unified picture.

iivalent and heavy meta ion concentrations. One can also explore community structtre
iith "live-dead" bacterial stains and fluorescent probes.

The identity of members of communities of microorganisms in natural environments,

heir distrbution, and the combined effects of their metabolisms on miera dissolution ar

ferrettd out all the glitches. WWB is deeply indebte to Vernon Hurst for pointing him

;urrently poorly understood. As noted elsewhere in this volume, extraordinarily powerful

nolecular techniques are now available to identify microbes (e.g. 16S rDNA analysis) ahd

clown the weaeringlorganoclay path. SAW thanks Bil Ullman for many yeas of help and
support. We also acknowledge Colleen Lavin and Ya Chen for cryomicroscopy support,

:hese can be applied to sediment, rock, and soil samples without culturing. Molecular

nformation ca be related to individual cens through the use of oligonucleotide probes

iilowing microbial eclogical information to be added to the mineraogical and geochemical

Barker, Welch, Banfield: Biochemical Weathering of Silcates

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421

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to

BavestreHo G, ArHo A. Benatti U. CelTano C. Cattaeo- Viet R. Cortesogno L. Gaggero L, Giovine M.

rant RR00570. Additional research support from the National Science Foundation

'ovided in par by the IMR, Madison, WI, through NIH Biomedical Research Technology
:Jrants EAR-950817l, EAR-9317082, CHE-9521731) and the Deparent of Energy
)E-FG02-93ER14328) is very gratefully acknowledged.

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