(1999) Berker. Review of Soluble Microbial Products

PII: S0043-1354(99)00022-6
Wat. Res. Vol. 33, No. 14, pp. 30633082, 1999

# 1999 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
0043-1354/99/$ - see front matter
www.elsevier.com/locate/watres
REVIEW PAPER
A REVIEW OF SOLUBLE MICROBIAL PRODUCTS (SMP)
IN WASTEWATER TREATMENT SYSTEMS
M
M
DUNCAN J. BARKER*
and DAVID C. STUCKEY**
Department of Chemical Engineering and Chemical Technology, Imperial College of Science,

Technology and Medicine, Prince Consort Road, London SW7 2BY, UK
(First received September 1998; accepted in revised form December 1998)
AbstractA review concerning the characterisation, production, modelling, signicance and implications of soluble microbial products (SMP) in wastewater treatment is presented. The precise denition
of SMP is open to debate, but is currently regarded as ``the pool of organic compounds that are
released into solution from substrate metabolism (usually with biomass growth) and biomass decay'',
although for anaerobic systems volatile fatty acids are not included as SMP. Some of the SMP have
been identied as humic and fulvic acids, polysaccharides, proteins, nucleic acids, organic acids, amino
acids, antibiotics, steroids, exocellular enzymes, siderophores, structural components of cells and products of energy metabolism. Crucially, SMP have been found to comprise the majority of soluble organic material in the euents from biological treatment processes and their presence is, therefore, of
particular interest in terms of achieving discharge consent levels for BOD and COD. SMP also exhibit
several characteristics, such as toxicity and metal chelating properties, which eect the performance of
the treatment system, and their presence has also been shown to adversely aect the kinetic activity and
the occulating and settling properties of sludge. This review outlines some important discoveries with
regard to the MW distribution, biodegradability and treatability of SMP and also the eect of process
parameters on their production. It also summarises the attempts at incorporating SMP formation into
the modelling of wastewater treatment. However, it concludes that the knowledge regarding SMP is far
from complete and that much work is still required to fully understand their contribution to the treatment process; some of these future research areas are then outlined. # 1999 Elsevier Science Ltd. All
rights reserved
Key wordssoluble microbial products (SMP), molecular weight distribution, euent, biodegradability,
chelating, toxicity, characterisation, process performance
AbbreviationsABR, anaerobic baed reactor, AMW, apparent molecular weight, BAP, biomass associated products, BMP, biochemical methane potential, BOD, biochemical oxygen demand, COD,
chemical oxygen demand, CSTR, continuously stirred tank reactor, ECP, extracellular polymers, GAC,
granular activated carbon, GPC, gel permeation chromatography, HRT, hydraulic retention time,
MLSS, mixed liquor suspended solids, MLVSS, mixed liquor volatile suspended solids, MW, molecular
weight, OLR, organic loading rate, PAC, powdered activated carbon, PACT, powdered activated carbon treatment, SBR, sequencing batch reactor, SMP, soluble microbial products, SOC, soluble organic
carbon, SON, soluble organic nitrogen, SRP, soluble residual products, SRT, sludge retention time,
THM, trihalomethane, TOC, total organic carbon, UAP, utilisation associated products, UASB, upow
anaerobic sludge blanket, UF, ultraltration, VSS, volatile suspended solids
INTRODUCTION
Euents from biological wastewater treatment systems contain a variety of soluble organic compounds, including residual degradable and non- or
slowly biodegradable inuent substrate, substrate
intermediates and end products, complex organic
compounds formed through condensation reactions
*Author to whom all correspondence should be addressed.
[Tel.: +44-171-594-5591;
Fax: +44-171-594-5604;
E-mail: d.stuckey@ic.ac.uk].
with both inuent organics and intermediate and

nal degradation products and SMP. The term
SMP has been adopted to dene the pool of organic compounds that are released into solution
from substrate metabolism (usually with biomass
growth) and biomass decay. The existence of residual microbial products produced by microbial
cultures involved in wastewater treatment was
demonstrated as early as 1961 (Ganey and
Heukelekian, 1961). Since then many researchers
(Chudoba, 1967; Chudoba et al., 1968a, b; Grady
3063
3064
Dencan J. Barker and David C. Stuckey
et al., 1972; Grady and Williams, 1975; Daigger

and Grady, 1977a, b; Baskir and Hansford, 1980;
Siber and Eckenfelder, 1980; Saunders and Dick,
1981; Parkin and McCarty, 1981a, b, c; Gaudy and
Blachly, 1985; Namkung and Rittmann, 1986;
Rittmann et al., 1987; Noguera et al., 1994,
Schiener et al., 1998) have shown that the majority
of the soluble organic matter in euents from biological treatment processes is actually SMP. Hence,
their presence is a matter of great interest not only
in terms of achieving current discharge standards,
but also because they eectively set the lower limit
for treatment.
Acknowledging the presence of SMP revolutionised the understanding of wastewater treatment
systems. Previously, models of wastewater treatment
systems had been based on the Monod model
which predicted that the euent concentration of
the rate limiting substrate should be independent of
the inuent substrate concentration. This did not
agree with observed measurements and the incorporation of SMP formation paved the way for
more accurate modelling of wastewater treatment.
Alongside the advances in modelling there has been
a growing understanding of how mixed bacterial
populations work and, with advances in chemical
identication methods, what these compounds are.
Most of the work has focused on SMP in aerobic
systems, but a handful of workers have also investigated SMP in anaerobic systems. The importance
of SMP in all types of wastewater treatment is now
fairly well accepted, but diculties still occur in trying to measure SMP and draw conclusions when
they are present in euents from plants treating
highly complex feeds. Hence, much of the work
regarding SMP has been done on pure cultures and
dened feeds. Translating this knowledge into
``real'' systems is, as yet, an uncompleted task.
Despite the obvious importance of SMP in wastewater treatment systems, and the increasing number
of publications, there has never been any attempt to
summarise all the information in a comprehensive
review. However, Rittmann et al. (1987) carried out
a critical evaluation of microbial product formation
in biological systems which covered: the measured
characteristics of SMP from biological processes;
results on the eect of sludge age (or specic
growth rate); and the literature on product formation during fermentation. Hence, the objective of
this paper is to review the currently available literature on SMP, focusing on: their denition; their origin; their identication; their MW, chelating
properties, biodegradability and toxicity characteristics; the factors which aect the production of
SMP and whether it is possible to minimise their
production by controlling these factors; their modelling in wastewater treatment; the comparison
between aerobic and anaerobic production and the
treatment (i.e. removal) of SMP. The current state
of the art will be summarised and, nally, a closing
section will address the future research needs with

regard to SMP.
THE DEFINITION OF SMP
Although the concept of microorganisms producing organic material during growth and endogenous decay is well accepted the term SMP has been
used by many authors without precise denition.
This is partly due to the diculty in identifying
SMP experimentally, but also to the complexities of
euent composition and actually tracing the origin
of the myriad compounds that exit a particular system. Boero et al. (1991) state that SMP result
``from intermediates or end products of substrate
degradation and endogenous cell decomposition'',
whereas Noguera et al. (1994) dene SMP ``as the
pool of organic compounds that result from substrate metabolism (usually with biomass growth)
and biomass decay during the complete mineralisation of simple substrates''. The inclusion of
``during the complete mineralisation of simple substrates'' in the denition is open to some debate.
Noguera et al. (1994) then insist that ``when a substrate is not completely mineralised, such as in fermentation reactions, the end-products of the
incomplete degradation of the substrate should not
be included in the denition of SMP, because, in
this case the end-products come directly from the
substrate, rather than having a microbial origin''.
Hence, they conclude that ``for anaerobic systems
intermediate compounds, such as volatile fatty
acids, should be excluded from the denition of
SMP because they are not of microbial origin''.
Although this appears somewhat of a contradiction
to call the intermediates not of microbial origin, the
opportunity to eliminate intermediate products
from SMP because they are the end-products of the
incomplete degradation of more complex compounds by specic groups of bacteria and the substrates for another group of microorganisms in the
anaerobic chain does have some practical validity,
particularly in terms of characterising the refractoriness of the euent. Kuo and Parkin (1996) and
Kuo et al. (1996) agree with this denition and for
the purposes of their research on glucose fed anaerobic systems dened SMP as:
SMP Soluble COD 1:07HAc 1:51HPr
1:82HBu 1:07Glu
where HAc=measured acetic acid
(mg/l);
HPr=measured
propionic
acid
(mg/l);
HBu=measured iso- and n-butyric acid (mg/l) and
Glu=measured glucose (mg/l).
The values 1.07, 1.51 and 1.82 are conversion factors based on the assumption of complete oxidation
of the volatile acids or glucose to CO2 and H2O.
This denition of SMP in anaerobic systems has
also been adopted by several other workers
Review of soluble microbial products
(Nachaiyasit and Stuckey, 1997; Schiener et al.,

1998).
Another approach adopted by several authors,
notably Chudoba (1985b) and Orhon and coworkers (Orhon et al., 1989; Artan et al., 1990;
Germirli et al., 1991), is to concentrate only on
SRP and thus be more concerned with the biodegradability of the material. If one only concentrates
on the residual material for the normal hydraulic
and sludge retention times used, then clearly the
degradation intermediates are eliminated from the
group because they are not refractory. This classication systems has its uses, particularly from a process engineering point of view, but it does not
satisfactorily address the biodegradability of non-intermediate soluble microbial products.
Chudoba (1985b) classied the organic compounds produced by activated sludge micro-organisms into three categories:
1. Compounds excreted by micro-organisms due to
their interaction with the environment.
2. Compounds produced as a result of substrate
metabolism and bacterial growth.
3. Compounds released during the lysis and degradation of micro-organisms.
Microbiologists classify microbial product formation into three categories: growth-synonymous;
growth-associated and growth-independent (Kono
and Asai, 1969; Pirt, 1969) and Chudoba (1985b)
states that ``if we apply this classication to organic
compounds produced by activated sludge also, then
those from the categories 1 and 3 mentioned above
are growth-independent products while those from
the second group are growth-synonymous and
growth-associated products'' although this appears
to be somewhat of a simplication. Namkung and
Rittmann (1986) grouped SMP into two dierent
categories based on the bacterial phase from which
they were derived:
1. UAP, i.e. SMP that are associated with substrate
metabolism and biomass growth and are produced at a rate proportional to the rate of substrate utilisation.
2. BAP, i.e. SMP that are associated with biomass
decay and are produced at a rate proportional to
the concentration of biomass.
. Using these categories they were able to successfully model substrate utilisation, SMP formation
and the removal of total soluble organic matter for
a biolm.
Whilst the debate of what is and what is not an
SMP is interesting, the actual denition of SMP is
of little interest to the practicing process engineer.
Their only concern is reaching the required discharge standard regardless of what type of material
is contained within the euent and from their per-
3065
spective the practical denition of SMP is any soluble material that leaves the euent from a
biological system that was not present in the inuent.
THE ORIGIN OF SMP
The most denitive list on the origin of SMP is

provided by Kuo (1993). He cites the following factors as causes of SMP production:
1. Concentration equilibrium: organisms excrete
soluble organic materials to establish a concentration equilibrium across the cell membrane
(Harold, 1972; Christensen, 1975; Payne, 1976).
2. Starvation: bacteria excrete organic materials
during starvation because they must obtain
energy for maintenance by endogenous respiration or metabolism of intracellular components
when the substrate is essentially absent (Dawes
and Ribbins, 1964; Burleigh and Dawes, 1967;
Boylen and Ensign, 1970).
3. Presence of energy source: the presence of an
increased concentration of exogenous energy
source can stimulate the excretion of SMP (Saier
et al., 1975; Neijssel and Tempest, 1976;
Thompson, 1976).
4. Substrate-accelerated death: sudden addition of a
carbon and energy source to bacteria starved for
carbon and energy may accelerate the death of
some bacteria. SMP may be produced as a result
of this process (Postgate and Hunter, 1964;
Dawes and Ribbins, 1964; Strange and Dark,
1965; Pirt, 1975).
5. Availability of required nutrient: if essential
nutrients are present in very low concentrations,
SMP may be produced to scavenge the required
nutrient (Neilands, 1967; Hutner, 1972; Pirt,
1975; Emery, 1982; Morel, 1983). Siderophores
are a typical example.
6. Relieving environmental stress: SMP are produced in response to environmental stress, such
as extreme temperature changes and osmotic
shocks (Nossal and Heppel, 1966; Heppel, 1967;
Smeaton and Elliot, 1967; Rogers, 1968). Kuo
(1993) also speculates that SMP are produced in
response to toxic substances.
7. Normal bacterial growth and metabolism: SMP,
such as exocellular enzymes, are not only produced during stressed conditions but also during
normal growth and metabolism (Herbert, 1961;
Demain et al., 1965; Saier et al., 1975).
IDENTIFICATION OF SMP
In general, a considerable portion of the euents

from wastewater systems is rather poorly dened
chemically. The need to identify specic compounds
<10 (65% strong acids)

<10
<5 (no simple sugars)

<5
010
065
trickling lter and

activated sludge
Euent
Ether extractables
Proteins
Amino acids
Carbohydrates and polysaccharides
Tannins and lignins
Alkyl benzene sulphonate (ABS)
Anionic detergents
Non-ionic detergents
Humic, fulvic and hymathomelanic acids
Volatile acids
Non-volatile acids
Neutral volatile compounds
Steroids
Optical brighteners
Organo-chlorine compounds
Unidentied
Also identied in low (<50 mg/l) concentrations
Bunch et al. (1961)
Reference
08.3
022.4
011.5
01.7
013.9
4050
trickling lter
Rebhun and Manka (1971)
4.6
0.2
5.1
3.2
1.6
5.4
11.8
3.1
0.8
0.5
<0.001
3.7
dialysable fraction
(i.e. MW<10 kDa)
1.7
54.3
glucose, fructose, sucrose, mannose,
allulose, xylose, ranose, formic acid,
acetic acid, propionic acid, butyric
acid, iso-butyric acid, iso-valeric acid,
caproic acid, uric acid, pyrene, perylene,
benzpyrenes, DDT
(pesticide), BHC (pesticide), dieldrin
(pesticide), coprostanol and cholesterol
non-dialysable fraction
(i.e. MW>10 kDa)
sewage euent
Painter (1973)
Table 1. Percentage composition of soluble organics (w/v) in euents from wastewater treatment systems
nonanoic acid, decanoic acid,

undecanoic acid, dodecanoic acid,
tetradecanoic acid, pentadecanoic acid,
palmitic acid, stearic acid, n-alkanes
C17H36C35H72, isopropyl benzene,
dodecyl benzene, napthalene,
methylnapthalene, diphenyl,
diphenylmethane, dioctylphthalate,
phenol and triethylphosphate
trickling lter, activated sludge and

stabilisation pond euents
Manka et al. (1974)
3066
present in the euents may seem of only academic

interest but a greater understanding of the precise
composition would enable a better discussion of
what exactly is an SMP and what is not. Several
researchers in the 1960s and 1970s tried to identify
individual compounds present in the euents and
their ndings are summarised in Table 1. Further
reports are available in the literature (Strange et al.,
1963; Demain et al., 1965; Mateles and Chian,
1969; McGregor and Finn, 1969; Thomas and Batt,
1969; Pavoni et al., 1972; DeWalle and Chian,
1974a, b; Saunders and Dick, 1981; Parkin and
McCarty, 1981a; Manka and Rebhun, 1982) that
have identied several other compounds of microbial origin such as humic and fulvic acids, polysaccharides, proteins, nucleic acids, organic acids,
amino acids, antibiotics, steroids, exocellular
enzymes, siderophores, structural components of
cells and products of energy metabolism. Recently,
Urbain et al. (1998) stated that UAP are mainly
small carbonaceous compounds derived from the
original substrate and that BAP are cellular macromolecules containing both carbon and nitrogen,
although the experimental evidence for this is not
denite.
Hejzlar and Chudoba (1986a, b) and Schiener et
al. (1998) concentrated on trying to identify the
high MW fraction present in euents. Hejzlar and
Chudoba (1986a, 1986b) found that all the polymers isolated from an activated sludge reactor contained sugars, amino sugars, uronic acids and
amino acids, indicating their heteropolysaccharidic
character. Schiener et al. (1998), performing a similar analysis on the high MW material from an
ABR, identied the high MW fraction as a heteropolysaccharide consisting of monosaccharides and
an amino sugar, although 9% of the hydrolysis products remained unidentied.
Although most of the research in this area has
appeared to emphasise the fact that all euents are
dierent essentially because all inuents are dierent, it may be that dierent euents will contain
some ``generic'' compounds (i.e. same SMP) and
therefore be similar in composition, however there
is no experimental evidence for this at present.
Separating those compounds that have entered the
system through the inuent and those that have
been produced by the system itself is not easy and
one must ask how useful this information is to the
operating facility. Many industries produce large
quantities of dicult to degrade material (``refractories'') and this has a signicant eect on the nal
euent that can be achieved; in these cases SMP
become irrelevant.
THE CHARACTERISTICS OF SMP
Engineers are generally most interested in collective parameters that can tell them something about
the total or overall performance of the system and
3067
hence much of the past research has focused on the

global characteristics of SMP. Parameters such as
MW distribution, biodegradability and toxicity are
of particular interest. MW distribution has been
shown to be important in assessing the eciency
and suitability of the process and removal technology to be employed (Manka and Rebhun, 1982;
Amy et al., 1987b), biodegradability is important
for the BOD assessment of euent, while toxicity is
important when considering the disposal of an euent.
MW distribution of SMP
There is no standardised procedure for determining the MW distribution of soluble organic compounds. This creates diculties in comparing results
from dierent studies and means that dierent
results serve only as a relative measure of MW distribution. Size distributions of soluble organic compounds are determined either as a continuous
distribution using GPC or as a discrete distribution
using UF membranes in stirred cells. The sizes of
these soluble organics are always referred to as
AMWs, since separations are calibrated with compounds of known MW, not size, but both techniques have several disadvantages (Amy et al.,
1987b; Logan and Jiang, 1990). For example,
during a chromatographic analysis, there should be
no chemical interaction between the column packing, the solvent (eluent), or the organic components.
This is because it has been found that some components pass through the column more rapidly than
calibration standards due to ion exclusion or complex formation, resulting in an overestimation of
the component MWs (Knuutinen et al., 1988),
while other components may be delayed by adsorption or electrostatic interaction with the column
packing and their MWs underestimated (Miles and
Brezonik, 1983). Also, chromatographic analysis
usually requires concentration by evaporation or
freeze-drying and these procedures may alter the
sizes of dissolved components. In ultraltration, the
diusive and advective transport of organics
through ultraltration membranes is inuenced by a
variety of factors, including membrane pore size
distribution, water temperature, cell pressure, solution pH and ionic strength, as well as molecule
size, shape and anity for the dierent membrane
materials (Logan and Jiang, 1990). In addition, the
performance of the membrane can be signicantly
aected if material is allowed to accumulate on the
membrane surface.
MW distributions of organics in samples can be
determined by either serial or parallel processing of
samples through an array of pressurised stirred cells
containing ultraltration membranes and the
schemes are illustrated in Fig. 1. According to
Logan and Jiang (1990), parallel processing of
samples in batch mode is preferred since they can
be run simultaneously (i.e. serial handling of l-
3068
Fig. 1. Schematic diagram of the processing schemes used to determine size distributions of dissolved
organics using batch ultraltration cells: (top) parallel processing; (bottom) serial processing.
trates is not required) and they observed larger

errors in size distributions when using serial processing as opposed to parallel sample processing. The
size distribution is calculated as a dierence in mass
concentration between permeates from cells containing membranes with dierent nominal MW cutos. A major advantage of ultraltration over
chromatographic methods is that a large sample
volume can be processed and recovered for further
characterisation. Amy et al. (1987b) compared GPC
and UF for determining MW distributions of
aquatic organic matter. They found that the two
methods gave somewhat dierent trends in the
AMW distribution in various water sources, with
GPC generally indicating a higher MW than UF
and GPC was found to be signicantly aected by
pH conditions. Urano et al. (1980) also concluded
that GPC using Sephadex gel could not generally
be used for the fractionation of organic pollutants
in water solely by MW, but that it was a useful
technique for separating various organic pollutants
based on chemical structure.
The MW distribution of nal euents from
wastewater treatment systems, and of SMP, has
been investigated by several researchers. The majority of the work has been on aerobic systems and
both UF and GPC have been used to nd the MW
distributions. The results from these studies are
summarised in Table 2. Recently, Confer and
Logan (1997a, b, 1998) considered the macromolecular aspects of wastewater treatment euents and
in particular the MW distribution of hydrolytic
fragments in solution during protein and polysaccharide degradation. They used UF to follow the
MW of the macromolecules during degradation and
showed that small MW compounds (<1 kDa) accumulated in solution during both polysaccharide and
protein degradation. Many workers have specically
investigated the MW distribution of SMP. Parkin
and McCarty (1981a) found that 50 to 60% of the
SON and soluble COD in aerobically treated and
untreated municipal wastewater had AMWs of less
than 1.8 kDa as measured by GPC. Namkung and
Rittmann (1986) found that SMP from the aerobic
treatment of phenol contained mainly high MW
compounds (70% of euent SOC was in the MW
range >1 kDa) even though phenol (MW=94 Da)
was fed as the sole organic carbon source to the
biolm reactor. Boero et al. (1996) used 14 C-labelled
compounds to investigate the MW distribution of
SMP in aerobic treatments of glucose and phenol.
They split the generation of SMP into three distinct
regions based upon: the direct transformation of
the original substrate (region I); the ``polymerisation'' of the lower MW SMP (region II) and the
endogenous decay of cells (region III). They found
that, on average, the trends were similar for both
substrates and indicated that the lower MW fraction (<1 kDa) SMP dominated region I but
decreased with time (>46 h) as these compounds
were ``polymerised'' to form the higher MW fractions. However, the phenol associated SMP tended
to be of a higher MW than the glucose associated
SMP. Kuo and Parkin (1996) performed work on
the MW distribution of anaerobic SMP from their
studies using anaerobic chemostats. They found the
distribution of SMP to show the same type of distribution as for aerobic systems, i.e. bimodal with
the majority of SMP having a MW less than 1 kDa
or greater than 10 kDa, while very little SMP had a
trickling lter and

activated sludge
activated sludge
activated sludge
activated sludge
not reported
activated sludge
trickling lter, activated

sludge, stabilization pond
trickling lter
activated sludge
contact stabilisation plant
activated sludge
activated sludge
not reported
activated sludge
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Domestic wastewater
Type of biological
treatment
Substrate
COD
TOC
COD
COD
parameter
characterising
organic content
ndings
most of organics (61%) fell in

MW>20 kDa range
60%: dialysable, 40%: nondialysable
60% dialysable, 40% nondialysable
>1 kDa: 85%, <1 kDa: 15%
UF
ndings
4150 kDa: 25%, <1.24 kDa: 75%

>10 kDa: 85%, 0.510 kDa: 15%
>0.7 kDa: 5067%, <0.7 kDa: 33
50%
GPC
TOC
>1.8 kDa: 10%, 0.781.8 kDa: 13%,

330780: 20%, <330: 57%
<50 kDa: 85%, 550 kDa: 8%, 1

5 kDa: 10%, 0.51 kDa: 18%,
<0.5 kDa: 57%
absorbance at 350 nm majority of fulvic and hymathomelanic
acids isolated from euents had MW
ranging from 15 kDa, whereas most
of the humic acid present was found in
the range <0.5 kDa
TOC
>5 kDa: 20.428.8%, 1.55 kDa: 0%,
0.71.5 kDa: 12.717.4%, <0.7 kDa:
58.562.2%
COD
>1.8 kDa: 43%, 0.81.8 kDa: 30%,
0.1650.8 kDa: 21%, <165: 6%
TOC
>5 kDa: 30%, 750: 13%, 310: 33%,
0.1 kDa: 7%, <0.1 kDa: 17%
TOC
>1.8 kDa: 20%, 0.781.8 kDa: 17%,
330780: 25%, 150330: 8%, 62150:
7%, 2662: 5%, <26: 18%
SON and COD
>1.8 kDa: 9% COD, 8% SON; 0.78
1.8 kDa: 16% COD, 11% SON; 340
780: 22% COD, 19% SON; 165340:
7% COD, 23% SON; <165: 6%
COD, 6% SON; COD recovery=60%,
SON recovery=67%
TOC
COD
TOC
refractive index
parameter
characterising
organic content
Table 2. MW distributions in wastewater treatment euents
van Steenderen and Malherbe

(1982)
(continued on next page)
Manka and Rebhun (1982)
Parkin and McCarty (1981a)
Hart (1980)
Sachdev and Clesceri (1978)
Keller et al. (1978)
Sachdev et al. (1976)
Manka et al. (1974)
DeWalle and Chian (1974b)
Painter (1973)
Zuckerman and Molof (1970)

Bender et al. (1970)
Levins (1971)
Bunch et al. (1961)
Refs.

3069
activated sludge
Simple and complex
Glucose
semi-continuous cultivation
SBR
activated sludge
Domestic and synthetic

wastewater
Synthetic feed
activated sludge
trickling lter
Domestic wastewater
Domestic and synthetic

wastewater
activated sludge, pure

oxygen activated sludge,
activated biolter
Type of biological
treatment
Domestic wastewater
Substrate
activated sludge euent contained

more TOC within <0.5 kDa range
while activated biolter contained
greatest proportion of >100 kDa
and 30100 kDa material; pure
oxygen euent was intermediate to
the other euents
10 kDa0.2 mm: 20%, 110 kDa:
18%, <1 kDa: 62%
MW distribution and nonadsorbable material signicantly
inuenced by SRT
slime organic matter contained low
and high MW subfractions, both
of which decreased as SRT was
increased from 0.8 to 4.8 d; for
SRT>4.8 d, high MW slime
decreased to 05% of total euent
COD and low MW slime increased
to 066% of total euent COD
MW covered the entire range from
<1 to >100 kDa; bimodal shape
with minimal amounts of SOC in
1025 kDa range for reactors with
complex feed and 110 kDa for
reactors with simple feed; <1 kDa
fraction generally the greatest in
untreated euents
the largest portion of SMP
consisted of <1 kDa compounds
while the 3010 kDa fraction
exhibited the smallest content
TOC
TOC
TOC
COD
COD
TOC
ndings
parameter
characterising
organic content
UF
Table 2 (continued )
COD
>50 kDa: 10%, 1050 kDa: 35%, 0.7

10 kDa: 16%, <0.7 kDa: 39%
ndings
parameter
characterising
organic content
GPC
Chudoba (1985a)
Pribyl et al. (1997)
Grady et al. (1984)
Saunders and Dick (1981)
Kim et al. (1976b)
Logan and Jiang (1990)
Amy et al. (1987a)
Refs.
3070
SBR
Papermill euent
various anaerobic reactors
ABR
Sucrose
Various
aerobic biolm
Phenol
aerobic batch well-mixed

reactors
anaerobic CSTR
Glucose
Glucose and phenol
Type of biological
treatment
Substrate
ndings
parameter
characterising
organic content
COD
concentration of SMP increased

with increasing SRT; bimodal
distribution; fraction of SMP with
MW>10 kDa increased with
increasing SRT;SRT of 15 days:
43% MW<1 kDa, 48%
MW>10 kDa; SRT of 25 days:
27% MW<1 kDa, 62%
MW>10 kDa; SRT of 40 days:
16% MW<1 kDa, 76%
MW>10 kDa
TOC
phenol degradation resulted in
more SMP than glucose; the MW
distributions for both similar;
Phenol: region I, 90%
MW<1 kDa; region II, 41%
MW<1 kDa; region III, 48%
MW>100 kDa; glucose: region I,
75% MW<1 kDa; region II, 56%
MW<1 kDa; region III, 50%
MW>100 kDa
scintillation counting MW<0.5 kDa less than 20%. 30

64% had MW>10 kDa; all
distributions bimodal
TOC
>100 kDa: 25% <1 kDa: 30%;
high MW material increases down
reactor
TOC
0.2 mm0.45 mm: 11%, 30 kDa
0.2 mm: 6%, 1030 kDa: 0%, 1

10 kDa: 73%, <1 kDa: 10%
COD
majority of material in all euents absorbance at 210, 256
MW<1 kDa
and 280 nm
parameter
characterising
organic content
UF
Table 2 (continued )
Namkung and Rittmann (1986)

Schiener et al. (1998)
Barker et al. (1999)
Franta et al. (1994)
Boero et al. (1996)
Kuo and Parkin (1996)
Refs.
ndings
majority of material in all euents

MW<1 kDa
GPC

3071
3072
MW between 1 and 10 kDa. Schiener et al. (1998)

examined the MW distribution of SMP in an ABR
and found that the SMP exhibited a bimodal distribution with 30% having MW<1 kDa and 25%
having MW>100 kDa. They also showed that large
MW compounds increased as a percentage of the
total SMP down the reactor.
The conclusions from all this work on MW distributions can be summarised as follows:
. A greater amount of high MW compounds are
found in many biological euents than in the
inuent.
. Biological euents contain compounds with a
broad spectrum of MW (<0.5 to >50 kDa).
. Inuents generally exhibit skewed non-normal
MW distributions with a predominance of the
very low MW fraction (<0.5 kDa), while euents generally follow bimodal patterns.
. The MW distribution of the euent is signicantly aected by the operating conditions of the
system, with higher MW material becoming more
evident at high SRTs.
. The MW distribution of the SMP is aected by
the substrate type.
Chelating properties of SMP

If metals are present in high levels in wastewater
treatment systems they may be toxic, while if they
are not present in sucient quantities there may be
a nutrition problem. Typical chelating functional
groups, such as carboxylates, hydroxyls, sulphydryls
(SH), phenols and amines, are found in SMP
(Kuo and Parkin, 1996). These chelating groups can
act as ligands and complex with metals commonly
found in wastewaters and sludges (e.g. copper, iron,
lead, nickel and zinc). Complexation of metals by
microbial chelators will generally alleviate the toxicity but may also make the metals less available to
bacteria as micronutrients (Callender and Barford,
1983a, b). Kuo and Parkin (1996) have shown that
anaerobic micro-organisms produce moderate concentrations of nickel-chelating SMP of relatively
low strength and moderate capacity when compared
to simple organic compounds (e.g. acetate, citrate,
etc.). They found that the amount of SMP produced in a 40 day SRT chemostat could chelate approximately 44 mg Ni l1 which is a substantial
concentration and, hence, conclude that SMP may
play a role in mitigating heavy metal toxicity. As
far as aerobic systems are concerned, Bender et al.
(1970) found fractions isolated from secondary sewage euents (particularly the high MW fraction)
showed copper metal binding capacity and the concentration of ligands in their samples ranged from
8 105 to 1 106 M.
Biodegradability of SMP
Another collective parameter of interest is biodegradability. Parkin and McCarty (1981a), Gaudy
and Blachly (1985), Barker et al. (1999) and
Schiener et al. (1998) have investigated the biodegradability of residual COD, whilst Obayashi and
Gaudy (1973) specically studied the degradability
of extracellular polysaccharides. The most denitive
results are reported by Gaudy and Blachly (1985),
who found that over 90% of the residual COD
measured in batch or continuous ow treatability
studies, while being the practical or engineering
non-biodegradable residual with respect to secondary treatment processes, is subject to biological
degradation. They used a semi-continuously fed
batch reactor which was fed daily to increase the
liquid concentration by 1000 mg l1 every day.
During the rst 32 days of feeding, 1570 mg
COD l1 of SMP built up. This build up represented about 5% conversion of glucose COD to
SMP COD. However, the residual soluble COD
declined to only 324 mg l1 by day 66, even though
new glucose was continually being fed. Thus,
almost all of the previously formed SMP, as well as
newly formed SMP, was degraded. Parkin and
McCarty (1981a) found that the biodegradable fraction of activated sludge euent SON varied, ranging from 0 to 60%. Schiener et al. (1998)
investigated the anaerobic biodegradability (by
means of the BMP assay (Owen et al., 1979)) of
various MW fractions from dierent compartments
in an ABR. All the MW fractions in the compartments investigated were found to be between 65
and 82% degradable. Barker et al. (1999) studied
the aerobic and anaerobic degradability of dierent
MW fractions from various euents from anaerobic treatment and found that generally the high
MW material was more readily degraded aerobically and the low MW was more readily degraded
anaerobically, although there were dierences from
euent to euent.
Hejzlar and Chudoba (1986a, 1986b) studied the
dierent polymers that are excreted into the cultivation medium. From the practical viewpoint it is
very important to determine which are readily
degradable and which are refractory and they
assumed that the polymers which are commonly
present in most microbial cells (e.g. nucleic acids,
peptidoglycans and phospholipids) are easily
degradable by many micro-organisms but that, on
the contrary, specic and unrepeatedly synthesised
polymers (e.g. extracellular heteropolysaccharides
or polysaccharidic components of lipopolysaccharides) are refractory. Hejzlar and Chudoba (1986a)
quantied their refractoriness as having a BOD rate
constant of 0.030.04 d1.
Recently, Namour and Muller (1998) proposed a
new physico-chemical technique based on the fractionation of organic material into hydrophobic and
basic, acid and neutral hydrophilic entities, to quantify the refractory organic matter from sewage treatment works. This is an alternative to the highly
sensitive bioassay techniques and allows the extraction of the major part of the refractory organic
matter in order to generate fractions available for
further physical, chemical or biological tests.
Toxicity of SMP
There is an increasing concern that euent toxicity may actually be created in the biological treatment process itself (Eckenfelder, 1988, 1994, 1995).
In other words, SMP may actually be more toxic
than the original organic compounds present in the
wastewater. Rappaport et al. (1979), using the
Ames test, showed a greater mutagenic response in
secondary euents than in that of the primary euent and, signicantly, some SMP have also been
found to be inhibitory to nitrication (Chudoba,
1985a). Ross et al. (1998) also performed an ecotoxicological assessment that revealed S. capricornutum
growth inhibition reached 80% while 90% of V.
scheri bioluminescence was aected due to the presence of SMP in a groundwater biolm. As SMP
production is a concentration related phenomena,
the problem becomes more severe with high
strength
wastewaters
(Eckenfelder,
1994).
Eckenfelder (1994) found that SMP with high MWs
strongly adsorb onto carbon and has proposed
using GAC as an eective tertiary treatment to
reduce the toxicity of euents. All this work has
been with aerobic treatment systems and no data
has been found concerning the toxicity of anaerobic
SMP.
Eect of SMP on process performance
In addition to contributing to the BOD and
COD of the euent and exhibiting chelating and
toxicity properties, SMP can have further implications on process performance, although the eect
of high concentrations of these products is not yet
fully known. Washington et al. (1970) observed that
accumulation of SMP in a cultivation medium was
accompanied by a decrease in specic respiration
rates and Chudoba (1985a) concluded from his studies that microbial waste products in high concentrations adversely aected the kinetic activity and
the occulating and settling properties of activated
sludge micro-organisms. Of these microbial waste
products, ECP, although strictly not soluble, are
believed to have the major inuence on the settling
and occulating properties of activated sludge
(Pavoni et al., 1972). Indeed, they are now manufactured articially to be used as alternatives to
other synthetic or natural water soluble polymers or
as novel polymers in thickening, suspending and
gelling applications (Pace and Righelato, 1980). It is
also believed that ECP play an important role in
the formation of anaerobic granules in the UASB
reactor (Jia et al., 1996a, b).
3073
PROCESS PARAMETERS WHICH AFFECT THE

PRODUCTION OF SMP
The physical, chemical and biological factors that

inuence the production of SMP have already been
outlined. However, of considerable concern for engineers designing and operating wastewater treatment systems is the eect of various process
parameters on the production of SMP. All the investigations regarding the eect of process parameters tend to point to the fact that a considerable
decrease in the residual COD can be achieved
through optimisation of the biological treatment
process itself, rather than by increasing the size of
the treatment plant. This must be the preferable
option as the latter solution results in greater
investment and higher operation and maintenance
costs without necessarily lowering the euent concentration (Franta et al., 1994).
Eect of feed strength, HRT, OLR and SRT on
SMP production
Several investigators have studied the eect of
feed strength, HRT, OLR and SRT on SMP production and these studies are summarised in Table
3. The main conclusions from this work are:
. SMP production increases as the inuent concentration (S0) increases.
. When normalised SMP production (SMP/S0) is
plotted against SRT, SMP/S0 appears to decrease
to a minimum and then increase again, indicating
the existence of an optimal SRT for minimising
the production of SMP. For aerobic systems this
optimum appears to exist between 2 and 15 days
(Baskir and Hansford, 1980; Rittmann et al.,
1987; Hao and Lao, 1988; Pribyl et al., 1997),
while for anaerobic systems the optimum appears
at approximately 25 days (Kuo et al., 1996).
. A certain optimum range of organic loads exists
in which it is possible to obtain minimum values
of SMP. The optimum organic load is in the
range of 0.31.2 g COD/g MLSS d or 0.20.8 g
BOD/g MLSS d. A substantial increase or
decrease above or below the optimum range
results in an increase of SMP. At high loads, the
sludge is overloaded and it is not able to remove
all organic substances from solution; at low loads
it is underfed, so that it decomposes and releases
organic matter into solution (Chudoba, 1967;
Baskir and Hansford, 1980; Pribyl et al., 1997).
Eect of substrate type on SMP production

Whether the substrate aects the quantity and
type of SMP produced is closely linked to whether
bacterial type aects the quantity of SMP. Hao and
Lao (1988) found from their experiments with pure
cultures that depending on the bacterial species
completely mixed, continuous ow activated sludge units with multisubstrate feed

of glucose, phenol and sulfanilic acid
laboratory scale activated sludge units with a synthetic feed of sugar, sodium
alginate and nutrients
laboratory scale activated sludge units with substrate of domestic and synthetic
wastewater
activated sludge with synthetic feed
Siber and Eckenfelder (1980)
Baskir and Hansford (1980)
Saunders and Dick (1981)
Schiener et al. (1998)
ABR with sucrose-nutrients substrate
SBR with substrate of synthetic wastewater
Pribyl et al. (1997)
anaerobic CSTR with glucose feed
Noguera et al. (1994)
anaerobic CSTR with acetate and glucose feeds. SRT maintained from 15 to 56 d
and OLR from 0.18 to 0.50 g COD/l d
SBR treating papermill waste
Franta et al. (1994)
Kuo et al. (1996)
chemostat pure cultures of Sphaerotilus species, S. natans and Pseudomonas species
Hao and Lao (1988)
Chudoba (1985b)
activated sludge under various conditions
ll-and-draw reactors fed on lactose
Daigger and Grady (1977a)
Parkin and McCarty (1981b)
continuous culture with multicomponent substrate
pure cultures of A. aerogenes and E. coli in chemostats with glucose as substrate
continuous degradation of aspartic acid, valine, tyrosine, phenol, pyrocatechol and

p-cresol
System studied
Grady and Williams (1975)
Grady et al. (1972)
Chudoba (1967)
Refs.
Main ndings
SMP amounted to 0.61% of inuent COD under optimum sludge load conditions;
optimum sludge load for minimum values of residual COD is in the range of 0.51.2 g
COD g MLSS1 d1
if the growth limiting substrate is dened as matter measured by COD then concentration
of growth-limiting substrate is not controlled by the growth rate alone and is not
independent of the concentration of substrate entering the reactor
concentration of substrate entering a CSTR without recycle has a signicant eect upon
the steady state concentration of substrate in the reactor
euent soluble COD linearly related to inuent substrate; majority of euent organic
matter of microbial origin; eect of HRT on euent COD signicant at 5% level but not
1% level (HRT varied from 46 to 22 h)
substrate removal rates decreased with increasing sludge ages and decreasing F/M ratios.
Variations in inuent organic strength resulted in changes in euent quality at constant
MLVSS
due to the presence of SMP the concentration of substrate in the feed exerts a signicant
eect upon the COD in the euent and there is an optimum sludge age for achieving
minimum euent COD given by: optimum growth rateA(feed COD)0.5
signicant improvements in euent organic quality occurred with increasing SRT as a
result of decreases in slime organic matter
the amount of SON resulting from biomass decay was a function of MLSS concentration
and SRT and accounted for 2050% of biologically produced SON
linear relationship existed between the refractory microbial products and the initial
substrate concentration when both were expressed in COD units for batch nonproliferating and proliferating, continuous with high and low mean cell residence time and
semi-continuous with separate aerobic sludge stabilisation systems; the slope and intercept
of the relationship depended on the mean cell residence time and the observed specic
growth rate
rate of SMP formation is an exponential function of dilution rate (D); when D approaches
zero, large quantities of SMP are produced; as D increases, the concentration decreases to
a minimum (which depended on bacterial species) but further increases in D result in a
signicant concentration of SMP
highest COD removal obtained at highest sludge age (20 d) and longest reaction period
(22 h); only about 10% of euent COD had a microbial origin
at 40 d retention time all euent COD was SMP; for shorter retention times the
concentration of SMP remained constant but comprised a smaller fraction of the soluble
euent COD
longer SRT resulted in higher levels of SMP; when normalised SMP production (SMP/S0)
is plotted against SRT, SMP/S0 appears to decrease to a minimum at 25 days and then
increase again, indicating the existence of an optimal SRT for the production of SMP
conrmed that the amount of SMP depended on sludge age, hydraulic retention time and
concentration gradients within the SBR; minimum SMP concentrations in the euents
were achieved at sludge ages from 5 to 15 days and at organic sludge loading rates from
0.3 to 0.6 kg COD kg1 MLSS d1
decreasing HRT (and increasing OLR) resulted in increased SMP
Table 3. Eect of feed strength, HRT, OLR and SRT on SMP production
3074
(and the dilution rate), the concentration of SMP

ranged from 4 to 9% of the initial substrate concentration. Boero et al. (1991) using a CSTR with phenol and glucose feeds showed that phenol resulted
in more SMP than glucose, but that the phenol related SMP was more biodegradable than glucose
SMP. Germirli et al. (1991) while assessing the soluble inert fraction of ve dierent industrial wastes
(pulp and paper, meat processing, antibiotics, textile
and dairy euents) with total soluble CODs ranging from 1000 to 9300 mg l1 found that the
amount and nature of microbial products was
dominated by the microbial culture, which diered
greatly in their study as the acclimation prior to the
experiments was with industrial euents of dierent
character. Thus, the evidence indicates that the type
of substrate and hence microbial population is
another factor inuencing the production of SMP.
However, the signicance of this is probably not so
important as most of the literature indicates that
biomass decay products account for most of the
SMP rather than substrate metabolism products
(Parkin and McCarty, 1981c; Chudoba, 1985b;
Noguera et al., 1994).
Eect of biomass concentration on SMP production
As discussed earlier, SMP production has been
shown to be closely linked to the quantity of biomass present. It is generally thought that SMP are
produced at a rate proportional to the concentration of the biomass due to the release of organic
material from cell lysis. Hence, an accumulation of
biomass in the system leads to an increased amount
of SMP and this is why an increase in euent COD
is observed at high sludge ages (Rittmann et al.,
1987; Hao and Lao, 1988). In addition, Parkin and
McCarty (1981c), when investigating the excretion
of compounds by activated sludge micro-organisms
to maintain equilibrium concentrations across the
cellular membrane, found the concentrations of
excreted compounds to be independent of activated
sludge concentration in the range 7 to 2390 mg l1.
However, they diered with individual types of activated sludge, varying from 0.05 to 0.32 mg l1 for
SON and from 1 to 8 mg l1 for COD.
Eect of temperature on SMP production
The eect of temperature on the production of
SMP is poorly covered in the literature. Parkin and
McCarty (1981c) found the concentration of compounds excreted to maintain equilibrium across the
cellular membrane to be independent of temperature but Sollfrank et al. (1992) studied the eect of
temperature on the release of soluble inert material
and concluded that the amount of this material
increased with decreasing process temperature.
Nachaiyasit and Stuckey (1997) and Schiener et al.
(1998) also observed the enhanced production of
SMP at low temperatures in an ABR. In addition
to the fact that SMP production increases with
3075
decreasing temperature, a decreasing temperature

will also cause a decrease in the rate of degradation
of SMP due to kinetic considerations.
Eect of reactor type on SMP production
There is conicting evidence concerning the inuence of reactor type on the amount and nature of
SMP produced by activated sludge micro-organisms. Pribyl et al. (1997) found that a continuous
ow system with a completely mixed aeration tank
produced consistently higher concentrations of
SMP than a SBR. However, Artan and Orhon
(1989) modelling the eect of reactor hydraulics
found that there was no practical dierence between
the performances of completely mixed and plug
ow activated sludge systems, because they produced similar amounts of microbial products under
similar operating conditions. Barker et al. (1999)
found that reactor type was important with respect
to the type of SMP produced when comparing a
number of anaerobic treatment euents. They
found that reactors with an high SRT and high
VSS, such as the ABR, tend to produce more high
MW material which is probably the result of cell
lysis. Another reactor where SMP are of particular
signicance is in the UASB reactor where SMP are
an important component in the formation of sludge
granules (Jia et al., 1996a, b).
MODELLING OF SMP
The rst models of biological wastewater processes were based on the Monod model and they
predicted that the euent concentration of the rate
limiting substrate should be independent of the
inuent substrate concentration. However, numerous measurements at treatment plants and from experimental systems demonstrated that the amount
of soluble material leaving in the euent was proportional to the inuent concentration. Hence, a
dierent approach to modelling the process was
taken that included the formation of microbial products. The incorporation of SMP into the modelling
of wastewater treatment has been summarised in
more detail by other authors (Daigger and Grady,
1977b; Namkung and Rittmann, 1986; Artan et al.,
1990) and so what is presented here is merely a
brief overview of the developments and a report on
the latest progress. The rst model to characterise
microbial product formation was proposed by
Luedeking and Piret (1959) for the fermentation of
glucose to lactic acid:

dSP
dXT
1
a
b 0 XT
dt
dt
where SP=SMP concentration (mg/l); XT=total
biomass concentration (mg/l); a=growth associated
product formation coecient and b'=biomass associated product formation coecient (T1).
3076
This expression classies SMP into two categories: (a) growth associated products (or UAP)
that are produced at a rate proportional to the rate
of substrate metabolism and (b) non-growth associated products (or BAP) formed as by-products of
cell auto-oxidation or lysis and produced at a rate
proportional to the concentration of the biomass.
This expression was further developed and used by
several workers (Eckho and Jenkins, 1967;
Daigger and Grady, 1977b; Baskir and Hansford,
1980; Sykes, 1981; Rittmann et al., 1987; Artan et
al., 1990). Some of these workers concentrated on
SRP which are non-degradable, whilst others
included the degradability of the SMP. Eckho and
Jenkins (1967) were the rst to apply the concept to
treatment kinetics and they concentrated on the
production of SRP. Later, Sykes (1981) claimed
that microbial products were degradable but at a
rate slower than their generation. Daigger and
Grady (1977b) dened growth-synonymous SMP as
a third category, whose formation kinetics were
described as being proportional to the cell concentration and to the square of the specic growth
rate, to account for the increased SMP production
at very low sludge ages, although Rittmann et al.
(1987) made the point that there is no evidence in
the literature of products being formed at a rate
proportional to the square of the specic growth
rate. Artan et al. (1990) modied the IAWPRC
``Task group model No. 1'' (Henze et al., 1987) to
include the production of residual material and
also degradable material which is degraded in the
same way as inuent substrate. Namkung and
Rittmann (1986) investigated SMP formation kinetics in a biolm reactor and developed an extended
steady state biolm model based on the two types
of SMP.
The relative importance of BAP as compared to
UAP has been observed by several authors.
Chudoba (1985b) only observed relatively low levels
of SMP during microbial growth phase experiments
conducted with very high initial substrate concentrations. Parkin and McCarty (1981b) also observed
that SON production as a result of substrate oxidation may be signicant, but that in most cases its
concentration is small with comparison with SON
produced due to organism decay or the SON produced to attain equilibrium concentrations with the
activated sludge organisms; this has led to further
dierences in the approaches to modelling of SMP.
Boero et al. (1991) modelled SMP on a macroscopic
basis (i.e. no separation of SMP into individual
compounds) by considering two regions: region I,
where the original substrate still exists and region
II, a semi-endogenous region, where none of the
original substrate exists. Huang and Cheng (1987)
used a double substrate model to simulate a typical
activated sludge plant. Their model predicted that
under transient conditions SMP represented only a
small fraction of the euent COD, but that this ob-
servation was reversed in the case of steady state

conditions. Orhon et al. (1989) proposed a model
for the formation of SRP that related SRP to the
hydrolysis of non-viable cellular materials in the
reactor in an attempt to solve the problem of global
VSS measurements not dierentiating between
viable biomass and non-viable particulate organic
matter, while Rittmann et al. (1987) modelled SMP
degradation according to a semi-empirical multicomponent degradation model. All these dierent
approaches vary greatly in terms of what types of
SMP are considered and how the kinetics should be
represented, but Noguera et al. (1994), using results
from a glucose fed anaerobic chemostat, found the
most successful model included both production
and degradation of UAP and BAP by rst order
terms. Another development was the incorporation
of the production and degradation of microbial
products from dierent bacterial groups and the inclusion of the mechanism of heterotrophic growth
on SMP produced by nitrifying bacteria (Furumai
and Rittmann, 1992). The most recent development
has been by Urbain et al. (1998) who have taken
the modelling one step further by using 16S rRNA
probe analysis to determine the populations of heterotrophs and nitriers and to compare the results
to the output from the multispecies model of
Furumai and Rittmann (1992), that integrates substrate removal kinetics and SMP production/consumption. This means that they have achieved an
integrated analysis of the activated sludge process
based on chemical, molecular biology and mathematical tools. The model successfully described
their system under both steady state and transient
conditions except for technical problems or sudden
variations in the wastewater composition.
From a slightly dierent angle, Orhon and coworkers (Germirli et al., 1991, 1993; Orhon et al.,
1992, 1993) have looked at methods of measuring
and incorporating soluble residual product formation into the treatment of various industrial
euents. Their work has shown that SMP can not
be ignored in the treatment of industrial wastewaters and have highlighted an area that requires
much more attention.
AEROBIC VS ANAEROBIC SMP
While it is clear that the majority of work on

SMP has been conducted on aerobic systems, there
is still a need to explore SMP production in anaerobic systems in more depth. Only a handful of
workers have investigated SMP in anaerobic systems (Kuo, 1993; Noguera et al., 1994; Kuo and
Parkin, 1996; Kuo et al., 1996; Schiener et al., 1998;
Barker et al., 1999). No study has directly compared aerobic and anaerobic systems but data is
available for indirect comparison and, interestingly,
when comparing their results with the available literature reports on aerobic production of SMP, Kuo
et al. (1996) found that the normalised production

of SMP appears to be lower in anaerobic systems
(0.2 to 2.5%) than in aerobic systems [3.1 2 0.4%
for cultures fed on glucose and 14.72 3.7% for cultures fed on phenol (Boero et al., 1991)]. Germirli
et al. (1993) also showed that anaerobic treatment
yields substantially lower residual COD levels than
what would be normally associated with wastewaters treated by single-stage aerobic treatment and
that there is some evidence that anaerobic residual
material is degradable aerobically. Chudoba (1985b)
also showed that the amount of refractory compounds, expressed as COD, released from 1 g of
aerobically degraded biomass varied from 15 to
25 mg g1, but that under anaerobic conditions the
specic value of COD produced was 15.7 mg g1.
Kuo et al. (1996) used enrichment cultures to
study the production of SMP during the anaerobic
degradation of acetate and glucose to methane in
chemostats. Signicantly, as mentioned in the section concerning the denition of SMP, Kuo et al.
(1996) do not consider the short chain volatile fatty
acids produced by the bacterial consortia during the
degradation to be part of the SMP because ``they
are not of microbial origin''. Production of SMP
increased as SRT increased for both acetate and
glucose fed systems and systems fed glucose produced higher levels of SMP than those fed acetate.
For both systems euent COD was mostly SMP.
Glucose fed systems had higher SMP/euent soluble COD ratios than the acetate fed chemostats
and the fraction of the euent soluble COD made
up of SMP increased with increasing SRT. Noguera
et al. (1994) reported results from steady state and
tracer experiments with labelled glucose and acetate
and showed that signicant amounts of SMP were
produced during the acidogenesis of glucose, but
that SMP did not accumulate during methanogenesis from acetate. In addition, at high retention
times (40 days), SMP comprised almost all of the
euent COD from the glucose fed chemostat. For
shorter retention times the SMP concentration
remains almost constant but its signicance in the
euent COD is reduced due to the accumulation of
volatile fatty acids. Hence, both Noguera et al.
(1994) and Kuo et al. (1996) agree that the production of SMP is higher in glucose fed systems
than those fed on acetate and Kuo et al. (1996)
have suggested several explanations. The mineralisation of glucose to CH4 and CO2 is more energy
yielding than the degradation of acetate to the same
end products. This results in a higher bacterial yield
and thus higher biomass levels, which should lead
to higher levels of SMP. Additionally, glucose will
support the growth of dierent groups of microrganisms (i.e. fermenters, acetogens and methanogens), whereas acetate will support predominantly
aceticlastic methanogens and Kuo et al. (1996)
expect that the more diverse population would produce higher levels of SMP.
3077
TREATMENT OF SMP
Even though decreasing the amount of SMP

appearing in the euents from biological wastewater treatment systems is theoretically possible
through optimisation of the process, it is inevitable
that some SMP will remain in the euent. The implications of SMP appearing in the euent are:
rstly, that in considering any post treatment
method one should be prepared to design the
removal method based on the removal of SMP and
not original substrate and, secondly, that SMP can
be precursors for THM or chlorinated organics formation when subjected to chlorination before discharge (Namkung and Rittmann, 1988). Several
investigators have studied the treatability of SMP
with advanced treatment techniques, such as activated carbon, synthetic resin adsorption, ozonation,
oxidation, coagulation and breakpoint chlorination
and all of these techniques have their associated literature. Of all the possible options the literature
tends to indicate that GAC is the most eective
method for the removal of SMP. Parkin and
McCarty (1975), investigating several methods (various oxidants, chemical coagulants, ion exchange
and GAC) for the removal of SON from euents,
found that SON was removed by varying degrees
by the dierent processes, but that the most ecient
was GAC adsorption (85% removal) and chemical
precipitation using high concentrations of ferric
chloride (70% removal). Similarly, Randtke and
McCarty (1979) evaluated the potential of a number
of individual and combined wastewater treatment
processes for the removal of soluble secondary euent organics from aerobic treatment and again concluded that GAC adsorption was generally the most
procient. However, Kim et al. (1976b) did nd
that the mean cell residence time signicantly
aected the MW distribution and the adsorptability
on GAC of the soluble organic material in the euent from a CSTR. Schultz and Keinath (1984)
observed that nearly 50% of SMP were adsorbed
onto PAC in a PACT system, but that only 4% of
the adsorbed SMP was biodegraded by the PACT
sludge demonstrating the refractory nature of the
SMP. Very little has been reported regarding the
post treatment of anaerobic euents with activated
carbon. Fernandez and Forster (1993) used GAC
successfully, but work by Kim et al. (1990), looking
at the eect of a variety of biological treatment
methods on COD adsorption, indicated that, for a
simulated metal cuttings wastewater, euent from
an anaerobic treatment of the wastewater (and
hence anaerobic SMP) appeared less adsorbable
than those from an anaerobic/aerobic euent and
an aerobic euent. Barker et al. (1999) also showed
that low MW materials (i.e. MW<1 kDa) from anaerobic treatments were the most dicult to adsorb
on GAC.
3078
Trgovcich et al. (1983) found that breakpoint

chlorination of activated sludge euents substantially altered the character of the organic materials
present. Among the eects were a reduction in molecular size, reduction in biodegradability and reduction in adsorptability. Watt et al. (1985) found
that ozonation signicantly changed the adsorbability of activated sludge euent organic matter and
increased the concentration of organic materials
which totally resisted removal by carbon adsorption. The process also reduced the concentration of
non-biodegradable organic matter in the euents
and reduced the fraction of organic matter with
high MW (i.e. MW>100 kDa) and increased the
fraction of low MW (i.e. MW<1 kDa). Finally,
Kim et al. (1976a) used synthetic resins to remove
the organic matter from euents and found that
although the process was highly pH dependent it
did oer some potential for the removal of certain
organic compounds.
SUMMARY
Based on this review of the literature the current

state of the art with regard to SMP can be summarised as follows:
. As a result of the diculty in measuring it, denitions of SMP are somewhat ambiguous and
depend on what viewpoint is taken. From an engineering perspective, the most widely accepted
denition is ``the pool of organic compounds that
result from substrate metabolism (usually with
biomass growth) and biomass decay''. For
aerobic systems this is usually quite clear, however, for anaerobic systems the intermediate short
chain fatty acids are excluded from the SMP. A
basic operational denition is any soluble material that appears in the euent that was not
present in the inuent.
. SMP have been classied into two groups: UAP
and BAP. UAP are associated with substrate
metabolism and biomass growth and are produced at a rate proportional to the rate of substrate utilisation, while BAP are associated with
biomass decay and are produced at a rate proportional to the concentration of biomass.
. SMP are produced across a wide range of MWs
(<0.5 to >50 kDa) and the MW distribution has
been shown to be signicantly aected by the
operating conditions with higher MW material
becoming more evident at higher SRT (>15 days
for anaerobic systems and >46 h for aerobic systems).
. SMP have been shown to exhibit metal chelating
properties in both aerobic and anaerobic systems
and they probably play a role in metal toxicity
and metal bioavailability.
. SMP have been shown to be biodegradable,

although the kinetics of degradation may be a lot
slower than simple substrates.
. SMP have been demonstrated to exhibit some
toxicity in aerobic biological systems.
. High concentrations of SMP may adversely aect
the kinetic activity and the occulating and
settling properties of activated sludge.
. Process parameters such as feed strength, HRT,
OLR, SRT, substrate type, biomass concentration, temperature and reactor type aect SMP
production, but there is considerable evidence
that through optimisation of the biological treatment process signicant decreases in SMP can
occur and hence the residual COD can be
reduced. This is a more preferable option than
increasing the size of the treatment plant, with its
associated increase in investment costs and higher
operation and maintenance costs.
. The modelling of SMP production in wastewater
treatment systems has been successfully accomplished with a number of slightly dierent
approaches. The most recent advance is the integration of modelling SMP production and degradation with bacterial populations identied using
16S rRNA probes.
. Some workers have shown that the normalised
production of SMP is less in anaerobic systems
(0.2 to 2.5%) than aerobic (3.1 to 14.7%) and it
has been demonstrated that more SMP were produced during acidogenesis than methanogenesis.
. SMP can be removed from euents using a variety of dierent technologies, but the most eective appears to be activated carbon.
FUTURE RESEARCH NEEDS
We now understand the importance of considering SMP in the treatment of all types of wastewaters, but there is still much to learn regarding the
role of SMP in wastewater treatment systems.
Work in the following areas is necessary in order to
gain a greater understanding of SMP:
. Some clarication of the denition of SMP.
Although process engineers may want to classify
the material based on properties rather than origin, it is important to be precise about what is
meant by an SMP and what is not. This is dependent on improving the analytical measurements
of SMP. SMP is currently measured by dierence
and the errors are large relative to the quantity
of SMP leading to diculties in drawing conclusions from small values. Ideally, results need
to be presented that precisely quantify the
amount of SMP from all the dierent sources.
. The chemical identication of many SMP compounds is still not easy, but the increased use of
sophisticated analytical techniques to isolate and

identify some of these compounds is needed. If
these compounds can be accurately identied
then it may be possible to examine how refractory the individual compounds are and to determine which SMP are the most dicult to
remove. Further analysis of how these particularly refractory compounds are produced may
lead to the possibility of optimising bacterial
populations through ``genetic engineering'' techniques to reduce SMP.
. Identify, from a biological perspective, the key
factors that inuence the production of SMP.
This would then help process engineers to control
the most critical factors in order to reduce the
amount of SMP.
. Standardisation of the MW distribution measurement (either UF or GPC) so that better comparisons can be made between results obtained from
dierent systems.
. To understand the relationship between MW distribution of SMP and process parameters such as
temperature and organic loading rate.
. Understand the chelating properties of SMP in
more depth. Do SMP truly help to alleviate
metal toxicity (and which metals in particular),
or do they make the metals less biologically available?
. To understand the relationship between toxicity
and SMP production. On the one hand there is
concern that euent toxicity can be caused by
SMP, but on the other there is speculation that
cells produce more SMP when exposed to toxic
compounds.
. To understand more fully the relationship
between high concentrations of SMP and kinetic
activity and sludge settling characteristics.
. To continue work on pure cultures to understand
the relative contributions of SMP from dierent
species in a mixed culture.
. In terms of modelling, the short term challenge
must be to produce a sophisticated model for anaerobic systems along the lines of those developed by Urbain et al. (1998) and to address the
diculty of incorporating SMP into the modelling
of industrial wastewater treatment. The long term
challenges are to provide a modelling tool for
engineers designing and operating all types of
wastewater treatment systems whereby, given the
feed characteristics, operating conditions and
bacterial populations, one could accurately predict
the amount of SMP produced even as far as predicting the euent in terms of individual compounds.
. Finally, while it would appear that the problem
of SMP is essentially of a biological nature, its
impact is most strongly manifested in the process
engineering world. Hence, the solution lies in
greater collaboration between the two elds
whereby biologists generate the information for
3079
the process engineers to be able to engineer a solution on the treatment plant scale.
AcknowledgementsThe authors would like to acknowledge the nancial support of the Engineering and Physical
Sciences Research Council (EPSRC) and the Water
Research Centre (WRc) and they would also like thank
Dr Jason Plumb for his help in preparing this review.
REFERENCES
Amy G. L., Bryant Jr. C. W. and Belyani M. (1987a)

Molecular weight distributions of soluble organic matter
in various secondary and tertiary euents. Water Sci.
Technol. 19, 529538.
Amy G. L., Collins M. R., Kuo C. J. and King P. H.
(1987b) Comparing gel permeation and ultraltration
for the molecular weight characterization of aquatic organic matter. J. AWWA 79(1), 4349.
Artan N. and Orhon D. (1989) The eect of reactor
hydraulics on the performance of activated sludge systems. II. The formation of microbial products. Water
Res. 23(12), 15191525.
Artan N., Orhon D. and Baykal B. B. (1990) Implications
of the task group model. I. The eect of initial substrate
concentration. Water Res. 24(10), 12591268.
Barker D. J., Mannucchi G. A., Salvi S. M. L. and
Stuckey D. C. (1999) Characterisation of soluble residual chemical oxygen demand (COD) in anaerobic
wastewater treatment euents. Water Res., in press.
Baskir C. I. and Hansford G. S. (1980) Product formation
in the continuous culture of microbial populations
grown on carbohydrates. Biotech. Bioeng. XXII, 1857
1875.
Bender M. E., Matson W. R. and Jordan R. A. (1970) On
the signicance of metal complexing agents in secondary
sewage euents. Environ. Sci. Technol. 4(6), 520521.
Boero V. J., Eckenfelder Jr. W. W. and Bowers A. R.
(1991) Soluble microbial product formation in biological
systems. Water Sci. Technol. 23, 10671076.
Boero V. J., Eckenfelder Jr. W. W. and Bowers A. R.
(1996) Molecular weight distribution of soluble microbial products in biological systems. Water Sci.
Technol. 34(56), 241248.
Boylen C. W. and Ensign J. C. (1970) Intracellular substrates for endogenous metabolism during long-term
starvation of rod and spherical cells of arthrobacter
crustallopoietes. J. Bact. 103, 578587.
Bunch R. L., Barth E. F. and Ettinger M. B. (1961)
Organic materials in secondary euents. J. WPCF
33(2), 122126.
Burleigh I. G. and Dawes E. A. (1967) Studies on the endogenous metabolism and senescence of starved sarcin
lutea. Biochem. J. 102, 236250.
Callender I. J. and Barford J. P. (1983a) Precipitation,
chelation and the availability of metals as nutrients in
anaerobic digestion. I. Methodology. Biotech. Bioeng.
XXV, 19471957.
Callender I. J. and Barford J. P. (1983b) Precipitation,
chelation and the availability of metals as nutrients in
anaerobic digestion. II. Applications. Biotech. Bioeng.
XXV, 19591972.
Christensen H. N. (1975) Biological Transport, 2nd ed.
W.A. Benjamin, Reading, MA.
Chudoba J. (1967) Residual organic matter in activated
sludge process euents. I. Degradation of saccharides,
fatty acids and amino acids under batch conditions.
Scientic Papers of the Institute of Chemical
Technology (Czech). Technol. Water F12, 3975.
3080
Chudoba J. (1985a) Inhibitory eect of refractory organic

compounds produced by activated sludge micro-organisms on microbial activity and occulation. Water Res.
19(2), 197200.
Chudoba J. (1985b) Quantitative estimation in COD units
of refractory organic compounds produced by activated
sludge microorganisms. Water Res. 19(1), 3743.
Chudoba J., Nemec M. and Nemcova B. (1968a) Residual
organic matter in activated sludge process euents. II.
Degradation of saccharides, fatty acids and amino acids
under continuous conditions. Scientic Papers of the
Institute of Chemical Technology (Czech). Technol.
Water F13, 2743.
Chudoba J., Prasil M. and Emmerova H. (1968b)
Residual organic matter in activated sludge process
euents. III. Degradation of amino acids and phenols
under continuous conditions. Scientic Papers of the
Institute of Chemical Technology (Czech). Technol.
Water F13, 4561.
Confer D. R. and Logan B. E. (1997a) Molecular weight
distribution of hydrolysis products during biodegradation of model macromolecules in suspended and biolm
cultures I. Bovine serum albumin. Water Res. 31(9),
21272136.
Confer D. R. and Logan B. E. (1997b) Molecular weight
distribution of hydrolysis products during biodegradation of model macromolecules in suspended and biolm
cultures II. Dextran and dextrin. Water Res. 31(9),
21372145.
Confer D. R. and Logan B. E. (1998) A conceptual model
describing macromolecule degradation by suspended
cultures and biolms. Water Sci. Technol. 37(45), 231
234.
Daigger G. T. and Grady Jr. C. P. L. (1977a) Factors
aecting euent quality from ll-and-draw activated
sludge reactors. J. WPCF 49, 23902396.
Daigger G. T. and Grady Jr. C. P. L. (1977b) A model
for the bio-oxidation process based on product formation concepts. Water Res. 11, 10491057.
Dawes E. A. and Ribbins D. W. (1964) Some aspects of
the endogenous metabolism of bacteria. Bact. Rev. 28,
126149.
Demain A. L., Burg R. W. and Hendlin D. (1965)
Excretion and degradation of ribonucleic acids by
Bacillus subtilis. J. Bact. 89, 640646.
DeWalle F. B. and Chian E. S. K. (1974a) Kinetics of formation of humic substances in activated sludge systems
and their eect on occulation. Biotech. Bioeng. XVI,
739755.
DeWalle F. B. and Chian E. S. K. (1974b) Removal of organic matter by activated carbon columns. J. Environ.
Eng. Div. ASCE 100(EE5), 10891104.
Eckenfelder Jr. W. W. (1988) Point toxics control for
industrial wastewaters. Civil Eng. Pract. 3, 98112.
Eckenfelder Jr. W. W. (1994) Alternative strategies for
meeting stringent euent guidelines. Water Sci. Technol.
29(8), 17.
Eckenfelder Jr. W. W. (1995) Biological treatability studies: new regulations require a new approach. Environ.
Prog. 14(3), 172175.
Eckho D. W. and Jenkins D. (1967) Activated Sludge
Systems Kinetics of the Steady and Transient States.
SERL Report, No. 67-12. Berkeley, CA.
Emery T. (1982) Iron metabolism in humans and plants.
Am. Sci. 70, 626632.
Fernandez N. and Forster C. F. (1993) An evaluation of
the options for secondary treatment of euents produced from the anaerobic digestion of simulated coee
wastewaters. Environ. Technol. 14, 485490.
Franta J., Helmreich B., Pribyl M., Adamietz E. and
Wilderer P. A. (1994) Advanced biological treatment of
papermill wastewaters; eects of operation conditions
on COD removal and production of soluble organic
compounds in activated sludge systems. Water Sci.

Technol. 30(3), 199207.
Furumai H. and Rittmann B. E. (1992) Advanced modelling of mixed populations of heterotrophs and nitriers
considering the formation and exchange of soluble microbial products. Water Sci. Technol. 26(34), 493502.
Ganey P. E. and Heukelekian H. (1961) Biochemical oxidation of the lower fatty acids. J. WPCF 11, 11691184.
Gaudy Jr. A. F. and Blachly T. R. (1985) A study of the
biodegradability of residual COD. J. WPCF 57(4), 332
338.
Germirli F., Orhon D. and Artan N. (1991) Assessment of
the initial inert soluble COD in industrial wastewaters.
Water Sci. Technol. 23, 10771086.
Germirli F., Orhon D., Artan N., Ubay E. and Gorgun E.
(1993) Eect of two-stage treatment on the biological
treatability of strong industrial wastes. Water Sci.
Technol. 28(2), 145154.
Grady Jr. C. P. L. and Williams D. R. (1975) Eects of
inuent substrate concentration on the kinetics of natural microbial populations in continuous culture. Water
Res. 9, 171180.
Grady Jr. C. P. L., Harlow L. J. and Riesing R. R. (1972)
Eects of growth rate and inuent substrate concentration on euent quality from chemostats containing
bacteria in pure and mixed culture. Biotech. Bioeng.
XIV, 391410.
Grady Jr. C. P. L., Kirsch E. J., Koczwara M. K.,
Trgovcich B. and Watt R. D. (1984) Molecular weight
distributions in activated sludge euents. Water Res.
18(2), 239246.
Hao O. J. and Lao A. O. (1988) Kinetics of microbial byproduct formation in chemostat pure cultures. J.
Environ. Eng. Div. ASCE 114(5), 10971115.
Harold F. M. (1972) Conservation and transformation of
energy by bacterial membranes. Bact. Rev. 36, 172230.
Hart O. O. (1980) Development and application of a technique for the determination of the molecular mass distribution of organic compounds in water. Prog. Water
Tech. 12, 525536.
Hejzlar J. and Chudoba J. (1986a) Microbial polymers in
the aquatic environment: I. Production by activated
sludge microorganisms under dierent conditions.
Water Res. 20(10), 12091216.
Hejzlar J. and Chudoba J. (1986b) Microbial polymers in
the aquatic environment: II. Isolation from biologically
non-puried and puried municipal waste water analysis. Water Res. 20(10), 12171221.
Henze M., Grady C. P. L., Jr., Gujer W., Marais G. V. R.
and Matsuo T. (1987) Activated Sludge Model No. 1.
IAWPRC Scientic and Technical Report No. 1.
Heppel L. (1967) Selective release of enzymes from bacteria. Science 156, 14511455.
Herbert H. (1961) The chemical composition of microorganisms as a function of their environment. Symp.
Soc. Gen. Microbiol. 11, 391416.
Huang J. Y. C. and Cheng M.-D. (1987) Transient responses incorporating products formation. J. Environ.
Eng. 113(4), 868880.
Hutner S. H. (1972) Inorganic nutrition. Ann. Rev.
Microbiol. 26, 313346.
Jia X. S., Furumai H. and Fang H. H. P. (1996a)
Extracellular polymers of hydrogen-utilising methanogenic and sulphate-reducing sludges. Water Res. 30(6),
14391444.
Jia X. S., Furumai H. and Fang H. H. P. (1996b) Yields
of biomass and extracellular polymers in four anaerobic
sludges. Environ. Technol. 17, 283291.
Keller J. V., Leckie J. O. and McCarty P. L. (1978)
Investigation of soluble organic nitrogen compounds in
municipal secondary euent. J. WPCF 50, 25222529.

Kim B. R., Snoeyink V. L. and Saunders F. M. (1976a)
Adsorption of organic compounds by synthetic resins.
J. WPCF 48(1), 120133.
Kim B. R., Snoeyink V. L. and Saunders F. M. (1976b)
Inuence of MCRT on adsorption. J. Environ. Eng.
Div. ASCE 102(EE1), 5570.
Kim B. R., Anderson S. G. and Zemla J. F. (1990) Eect
of biological treatments on COD adsorption. Water
Res. 24(4), 457461.
Knuutinen J., Virkki L., Mannila P., Mikkelson P.,
Paasivirta J. and Herve S. (1988) High-performance
liquid chromatographic study of dissolved organic matter in natural waters. Water Res. 22(8), 985990.
Kono T. and Asai T. (1969) Kinetics of fermentation process. Biotech. Bioeng. XI, 293321.
Kuo W. C. (1993) Production of soluble microbial chelators and their impact on anaerobic treatment, Ph.D.
thesis, University of Iowa, Iowa City.
Kuo W. C. and Parkin G. F. (1996) Characterization of
soluble microbial products from anaerobic treatment by
molecular weight distribution and nickel-chelating properties. Water Res. 30(4), 915922.
Kuo W. C., Sneve M. A. and Parkin G. F. (1996)
Formation of soluble microbial products during anaerobic treatment. Water Environ. Res. 68, 279285.
Levins P. L. (1971) Characterization and separation of secondary euent compounds by molecular weight. A.D.
Little, E.P.A. Project 16020 FEN 03/71.
Logan B. E. and Jiang Q. (1990) Molecular size distributions of dissolved organic matter. J. Environ. Eng.
Div. ASCE 116(6), 10461062.
Luedeking R. and Piret E. C. (1959) A kinetic study of
lactic acid fermentation batch process at controlled pH.
J. Biochem. Microbiol. Tech. Eng. 1(4), 393412.
Manka J. and Rebhun M. (1982) Organic groups and molecular weight distribution in tertiary euents and renovated waters. Water Res. 16, 399403.
Manka J., Rebhun M., Mandelbaum A. and Bortinger A.
(1974) Characterization of organics in secondary euents. Environ. Sci. Technol. 8(12), 10171020.
Mateles R. I. and Chian S. K. (1969) Kinetics of substrate
uptake in pure and mixed cultures. Environ. Sci.
Technol. 3, 569574.
McGregor W. C. and Finn R. K. (1969) Factors aecting
the occulation of bacteria by chemical additives.
Biotech. Bioeng. 11, 127138.
Miles C. J. and Brezonik P. L. (1983) High-performance
size exclusion chromatography of aquatic humic substances. J. Chromatogr. 259, 499503.
Morel F. M. M. (1983) Principles of Aquatic Chemistry.
John Wiley Interscience, New York.
Nachaiyasit S. and Stuckey D. C. (1997) Eect of low
temperatures on the performance of an anaerobic
baed reactor (ABR). J. Chem. Tech. Biotech. 69, 276
284.
Namkung E. and Rittmann B. E. (1988) Eects of SMP
on biolm-reactor performance. J. Environ. Eng. Div.
ASCE 114(1), 199210.
Namkung E. and Rittmann B. E. (1986) Soluble microbial
products (SMP) formation kinetics by biolms. Water
Res. 20(6), 795806.
Namour Ph. and Muller M. C. (1998) Fractionation of organic matter from wastewater treatment plants before
and after a 21-day biodegradability test: a physical
chemical method for measurement of the refractory part
of euents. Water Res. 32(7), 22242231.
Neijssel O. M. and Tempest D. W. (1976) The role of
energy-spilling reactions in the growth of Klebsiella
Aerogenes NCTC 418 in aerobic chemostat culture.
Arch. Microbiol. 110, 305311.
Neilands J. B. (1967) Hydroxamic acids in nature. Science
156, 14431447.
3081
Noguera D. R., Araki N. and Rittmann B. E. (1994)

Soluble microbial products (SMP) in anaerobic chemostats. Biotech. Bioeng. 44, 10401047.
Nossal N. G. and Heppel L. A. (1966) The release of
enzymes by osmotic shock from E. coli in exponential
phase. J. Biol. Chem. 241(13), 30553062.
Obayashi A. W. and Gaudy Jr. A. F. (1973) Aerobic
digestion of extracellular microbial polysaccharides. J.
WPCF 45, 15841594.
Orhon D., Artan N. and Cimc it Y. (1989) The concept of
soluble residual product formation in the modelling of
activated sludge. Water Sci. Technol. 21, 339350.
Orhon D., Artan N., Buyukmurat S. and Gorgun E.
(1992) The eect of residual COD on the biological
treatability of textile wastewaters. Water Sci. Technol.
26(34), 815825.
Orhon D., Gorgun E., Germirli F. and Artan N. (1993)
Biological treatability of dairy wastewaters. Water Res.
27(4), 625633.
Owen W. F., Stuckey D. C., Healy Jr. J. B., Young L. Y.
and McCarty P. L. (1979) Bioassays for monitoring biochemical methane potential and anaerobic toxicity.
Water Res. 13, 485492.
Pace G. W. and Righelato R. C. (1980) Production of
extracellular microbial polysaccharides. Adv. Biol. Eng.
15, 4170.
Painter H. A. (1973) Organic compounds in solution in
sewage euents, Chem. Ind. September, 818822.
Parkin G. F. and McCarty P. L. (1975) Characteristics
and removal of soluble organic nitrogen in treated euents. Prog. Water Tech. 7(34), 435445.
Parkin G. F. and McCarty P. L. (1981a) A comparison of
the characteristics of soluble nitrogen in untreated and
activated sludge treated wastewaters. Water Res. 15,
139149.
Parkin G. F. and McCarty P. L. (1981b) Production of
soluble organic nitrogen during activated sludge treatment. J. WPCF 53(1), 99112.
Parkin G. F. and McCarty P. L. (1981c) Sources of soluble organic nitrogen in activated sludge euents. J.
WPCF 53(1), 8998.
Pavoni J. L., Tenney M. W. and Echelberger Jr. W. F.
(1972) Bacterial exocellular polymers and biological occulation. J. WPCF 44, 414431.
Payne J. W. (1976) Peptides and microorganisms. Adv.
Microb. Physiol. 13, 55113.
Pirt S. J. (1969) Microbial growth and product formation.
Symp. Soc. Gen. Microbiol. 19, 199221.
Pirt S. J. (1975) Principles of Microbe and Cell Cultivation.
Blackwell Scientic, Oxford.
Postgate J. R. and Hunter J. R. (1964) Accelerated death
of Aerobacter aerogenes starved in the presence of
growth-limiting substrates. J. Gen. Microbiol. 34, 459
473.
Pribyl M., Tucek F., Wilderer P. A. and Wanner J. (1997)
Amount and nature of soluble refractory organics produced by activated sludge micro-organisms in sequencing batch and continuous ow reactors. Water Sci.
Technol. 35(1), 2734.
Randtke S. J. and McCarty P. L. (1979) Removal of soluble secondary euent organics. J. Environ. Eng. Div.
ASCE 105(EE4), 727743.
Rappaport S. M., Richard M. G., Hollstein M. C. and
Talcott R. E. (1979) Mutagenic activity in organic
wastewater concentration. Environ. Sci. Technol. 13,
957961.
Rebhun M. and Manka J. (1971) Classication of organics
in secondary euents. Environ. Sci. Technol. 5(7), 606
609.
Rittmann B. E., Bae W., Namkung E. and Lu C.-J. (1987)
A critical evaluation of microbial product formation in
biological processes. Water Sci. Technol. 19, 517528.
3082
Rogers D. (1968) Osmotic pools in Escherichia coli.

Science 159, 531532.
Ross N., Deschenes L., Bureau J., Clement B., Comeau Y.
and Samson R. (1998) Ecotoxicological assessment and
eects of physicochemical factors on biolm development in groundwater conditions. Environ. Sci. Technol.
32, 11051111.
Sachdev D. R. and Clesceri N. L. (1978) Eects of organic
fractions from secondary euents on Selenastrum capricornutum (Kutz). J. WPCF 50, 18101820.
Sachdev D. R., Ferris J. J. and Clesceri N. L. (1976)
Apparent molecular weights of organics in secondary
euents. J. WPCF 48(3), 570579.
Saier M. H., Feucht B. U. and McCaman M. T. (1975)
Regulation of intracellular adenosine cyclic 3':5'-monophosphate levels in Escherichia coli and Salmonella
typhimurium. J. Biol. Chem. 250(19), 75937601.
Saunders F. M. and Dick R. I. (1981) Eect of mean-cell
residence time on organic composition of activated
sludge euents. J. WPCF 53(2), 201215.
Schiener P., Nachaiyasit S. and Stuckey D. C. (1998)
Production of soluble microbial products (SMP) in an
anaerobic baed reactor: composition, biodegradability
and the eect of process parameters. Environ. Technol.
19, 391400.
Schultz J. R. and Keinath T. M. (1984) Powdered activated carbon treatment process mechanisms. J. WPCF
56(2), 143151.
Siber S. and Eckenfelder Jr. W. W. (1980) Euent quality
variation from multicomponent substrates in the activated sludge process. Water Res. 14, 471476.
Sollfrank U., Kappeler J. and Gujer W. (1992)
Temperature eects on wastewater characterization and
the release of soluble inert organic material. Water Sci.
Technol. 25(6), 3341.
Smeaton J. R. and Elliot W. H. (1967) Selective release of
ribonuclease inhibitor from B. subtilis cells by cold
shock treatment. Biochem. Biophys. Res. Commun.
26(1), 7581.
Strange R. E. and Dark F. A. (1965) Substrate-accelerated

death of Aerobacter aerogenes. J. Gen. Microbiol. 39,
215228.
Strange R. E., Wade H. E. and Ness A. G. (1963) The catabolism of proteins and nucleic acids in starved
Aerobacter aerogenes. Biochem. J. 86, 197203.
Sykes R. M. (1981) Limiting nutrient concept in activated
sludge models. J. WPCF 53, 12131218.
Thomas T. D. and Batt R. D. (1969) Degradation of cell
constituents by starved Streptococcus lactis in relation
to survival. J. Gen. Microbiol. 58, 347362.
Thompson J. (1976) Characteristics and energy requirements of an A-aminoisobutyric acid transport system in
Streptococcus lactis. J. Bact. 127(2), 719730.
Trgovcich B., Kirsch E. J. and Grady Jr. C. P. L. (1983)
Characteristics of activated sludge euents before and
after breakpoint chlorination. J. WPCF 55(7), 966976.
Urano K., Katagiri K. and Kawamoto K. (1980)
Characteristics of gel chromatography using sephadex
gel for fractionation of soluble organic pollutants.
Water Res. 14, 741745.
Urbain V., Mobarry B., de Silva V., Stahl D. A.,
Rittmann B. E. and Manem J. (1998) Integration of
performance, molecular biology and modeling to
describe the activated sludge process. Water Sci.
Technol. 37, 223229.
van Steenderen R. A. and Malherbe A. (1982) The molecular mass distribution of organic compounds in activated sludge plant euent determined by means of gel
permeation chromatography. Water Res. 16, 745748.
Washington D. R., Clesceri L. S., Young J. C. and Hardt
F. W. (1970) Inuence of microbial waste products on
the metabolic activity of high solids activated sludge. In
Proceedings of 24th Purdue Industrial Waste Conference.
Purdue University, West Lafayette, IN, pp. 11031117.
Watt R. D., Kirsch E. J. and Grady Jr. C. P. L. (1985)
Characteristics of activated sludge euents before and
after ozonation. J. WPCF 57(2), 157166.
Zuckerman M. M. and Molof A. H. (1970) High quality
reuse water by chemicalphysical wastewater treatment.
J. WPCF 42(3 (Part 1)), 437456.

(1999) Berker. Review of Soluble Microbial Products

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

(1999) Berker. Review of Soluble Microbial Products

Uploaded by

Copyright:

Available Formats

PII: S0043-1354(99)00022-6

Wat. Res. Vol. 33, No. 14, pp. 30633082, 1999

Department of Chemical Engineering and Chemical Technology, Imperial College of Science,

with both inuent organics and intermediate and

Dencan J. Barker and David C. Stuckey

et al., 1972; Grady and Williams, 1975; Daigger

section will address the future research needs with

THE DEFINITION OF SMP

Review of soluble microbial products

(Nachaiyasit and Stuckey, 1997; Schiener et al.,

The most denitive list on the origin of SMP is

In general, a considerable portion of the euents

<10 (65% strong acids)

<5 (no simple sugars)

trickling lter and

Bunch et al. (1961)

Rebhun and Manka (1971)

nonanoic acid, decanoic acid,

trickling lter, activated sludge and

Manka et al. (1974)

Review of soluble microbial products

present in the euents may seem of only academic

hence much of the past research has focused on the

Dencan J. Barker and David C. Stuckey

trates is not required) and they observed larger

trickling lter and

trickling lter, activated

contact stabilisation plant

most of organics (61%) fell in

60%: dialysable, 40%: nondialysable

60% dialysable, 40% nondialysable

>1 kDa: 85%, <1 kDa: 15%

4150 kDa: 25%, <1.24 kDa: 75%

>1.8 kDa: 10%, 0.781.8 kDa: 13%,

<50 kDa: 85%, 550 kDa: 8%, 1

Table 2. MW distributions in wastewater treatment euents

van Steenderen and Malherbe

Manka and Rebhun (1982)

Parkin and McCarty (1981a)

Sachdev and Clesceri (1978)

Keller et al. (1978)

Sachdev et al. (1976)

Manka et al. (1974)

DeWalle and Chian (1974b)

Zuckerman and Molof (1970)

Bunch et al. (1961)

Review of soluble microbial products

Simple and complex

Domestic and synthetic

Domestic and synthetic

activated sludge, pure

activated sludge euent contained

>50 kDa: 10%, 1050 kDa: 35%, 0.7

Pribyl et al. (1997)

Grady et al. (1984)

Saunders and Dick (1981)

Kim et al. (1976b)

Logan and Jiang (1990)

Amy et al. (1987a)

various anaerobic reactors

aerobic batch well-mixed

Glucose and phenol

concentration of SMP increased

scintillation counting MW<0.5 kDa less than 20%. 30