Pedosphere 26(5): 577591, 2016

doi:10.1016/S1002-0160(15)60068-6
ISSN 1002-0160/CN 32-1315/P
c 2016 Soil Science Society of China
Published by Elsevier B.V. and Science Press

Soil Microbiological Activity and Carbon Dynamics in the Current

Climate Change Scenarios: A Review

Javid A. SOFI1, , Aabid H. LONE1 , Mumtaz A. GANIE1 , Naseer A. DAR2 , Sajad A. BHAT3 , Malik MUKHTAR4 ,
Mohd Ashraf DAR1 and Shazia RAMZAN1
1 Division of Soil Science, Faculty of Agriculture, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir
(SKUAST-K), Shalimar 190025 (India)
2 Division of Agronomy, Faculty of Agriculture, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir

(SKUAST-K), Shalimar 190025 (India)

3 Section of Plant Physiology, Division of Post-Harvest Technology (PHT), Sher-e-Kashmir University of Agricultural Sciences and

Technology of Kashmir (SKUAST-K), Shalimar 190025 (India)

4 Division of Entomology, Faculty of Agriculture, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir

(SKUAST-K), Shalimar 190025 (India)

(Received March 3, 2016; revised June 8, 2016)

ABSTRACT
Microbial activities are aected by a myriad of factors with end points involved in nutrient cycling and carbon sequestration issues.
Because of their prominent role in the global carbon balance and their possible role in carbon sequestration, soil microbes are very
important organisms in relation to global climate changes. This review focuses mainly on the responses of soil microbes to climate
changes and subsequent eects on soil carbon dynamics. An overview table regarding extracellular enzyme activities (EAA) with
all relevant literature data summarizes the eects of dierent ecosystems under various experimental treatments on EAA. Increasing
temperature, altered soil moisture regimes, and elevated carbon dioxide signicantly aect directly or indirectly soil microbial activities.
High temperature regimes can increase the microbial activities which can provide positive feedback to climate change, whereas lower
moisture condition in pedosystem can negate the increase, although the interactive eects still remain unanswered. Shifts in soil
microbial community in response to climate change have been determined by gene probing, phospholipid fatty acid analysis (PLFA),
terminal restriction length polymorphism (TRFLP), and denaturing gradient gel electrophoresis (DGGE), but in a recent investigations,
omic technological interventions have enabled determination of the shift in soil microbe community at a taxa level, which can provide
very important inputs for modeling C sequestration process. The intricacy and diversity of the soil microbial population and how it
responds to climate change are big challenges, but new molecular and stable isotope probing tools are being developed for linking
uctuations in microbial diversity to ecosystem function.
Key Words: carbon cycling, carbon dioxide, carbon exchange, carbon sequestration, microbe community, soil enzymes, soil moisture,
soil temperature

Citation: So J A, Lone A H, Ganie M A, Dar N A, Bhat S A, Mukhtar M, Dar M A, Ramzan S. 2016. Soil microbiological activity
and carbon dynamics in the current climate change scenarios: A review. Pedosphere. 26(5): 577591.

INTRODUCTION in, 2008). Terrestrial ecosystems release and absorb

The ongoing climate changes caused by anthro-
pogenic activities include emissions of 292 Pg C from
the combustion of fossil fuels (Holdren, 2008) and at
136 30 Pg C from land-use change, deforestation,
and soil cultivation (Houghton et al., 2001). It is very
important to understand the biological mechanism
regulating the carbon exchanges between land, oceans,
and atmosphere and how these exchanges will respo-
nd to climate changes through climate-ecosystem fe-
edbacks which could amplify or attenuate regional
or global climate changes (Heimann and Reichste-
greenhouse gases (GHGs) like carbon dioxide (CO2 ),
methane, and nitrous oxide, and also act as a sink while
storing carbon (C) in vegetation and soil (Schimel et
al., 1994). Sink activity of soil is aected by many fac-
tors including natural and anthropogenic disturbances
(Magnani et al., 2007), agricultural land use (Smith
et al., 2008), nitrogen (N) enrichment (Beedlow et al.,
2004), sulphur (S) deposition (Monteith et al., 2007),
and changes in atmosphere ozone concentration (Sitch
et al., 2007). Our knowledge of the assimilatory compo-
nent (photosynthesis) of the C cycle and its responses
to climate changes is well advanced (Bahn et al., 2008);

Corresponding author. E-mail: ahmadso12@gmail.com.

578
however, there are considerable gaps in our under-
standing of the responses of soil respiration (Trumbore,
2006). This lack of understanding of soil respiration
and its sensitivity to climate changes stems from the
fact that it is regulated by a number of complex intera-
ctions and feedbacks from climate, plants, their her-
bivores and symbionts, and free-living heterotrophic
soil microbes (Wardle et al., 2004; Hogberg and Read,
2006; De Deyn et al., 2008).
Soil microbial communities are responsible for the
cycling of C and nutrients in ecosystems and their ac-
tivities are regulated by biotic and abiotic factors such
as the quantity and quality of litter inputs, tempera-
ture, and moisture. Atmospheric and climatic changes
will impact both abiotic and biotic drivers in ecosys-
tems and the responses of ecosystems to these changes.
Feedbacks from ecosystem to the atmosphere may also
be regulated by soil microbial communities (Bardgett
et al., 2008). Although microbial communities regulate
important ecosystem processes, it is often unclear how
the abundance and composition of microbial commu-
nities correlate with climatic perturbations and inter-
act to aect ecosystem processes. As such, much of
the ecosystem climate change research conducted to
date has focused on macroscale responses to clima-
tic changes such as changes in plant growth (Nor-
by et al., 2001, 2004), plant community composition
(Bakkenes et al., 2002), and coarse-scale soil processes
(Emmett et al., 2004; Franklin et al., 2009; Garten et
al., 2008). Responses to climate change have been ad-
dressed to often targeted gross parameters, such as mi-
crobial biomass, enzymatic activity, and basic micro-
bial community proles (Zak et al., 1996, 2000; Janus
et al., 2005; Kuever et al., 2005; Kandeler et al., 2006;
Haaseet al., 2008).
The climatic variables such as atmospheric CO2
concentration, precipitation regimes, temperature can
potentially have both direct and indirect impacts on
soil microbial communities. However, the direction and
magnitude of these responses are uncertain. For exa-
mple, the response of soil microbial communities to
changes in atmospheric CO2 concentrations can be
positive or negative, and consistent overall trends be-
tween sites and studies have not been observed (Janus
et al., 2005; Lipson et al., 2005; Lipson et al., 2006;
Lesaulnier et al., 2008; Austin et al., 2009). Precipi-
tation and soil moisture changes may increase or de-
crease the ratio of bacteria to fungi, as well as shift
their community composition (Schimel et al., 1999;
Chen et al., 2007; Williams, 2007). Increasing tem-
peratures can increase microbial activity, processing,
and turnover, causing the microbial community to shift
J. A. SOFI et al.
in favor of representatives adapted to higher tempera-
tures and faster growth rates (Zogg et al., 1997; Zak
et al., 1999; Pettersson and Baath, 2003; Zhang et
al., 2005; Bradford et al., 2008). Single-factor climate
change studies described above have enabled better un-
derstanding how microbial communities may respond
to any one factor, but how multiple climate change
factors interact with each other to inuence microbial
community responses is poorly understood. For exam-
ple, elevated atmospheric CO2 concentration and pre-
cipitation changes might increase soil moisture in an
ecosystem, but this increase may be counteracted by
warming (Dermody et al., 2007).
Assays of extracellular enzymes activity (EEA)
have become one of the important tools for assessing
microbial responses to climate changes (Weedon et al.,
2011). Prolonged drought, high temperature, elevated-
CO2 concentration, etc., are the main actors in climate
change and it has been reported that in Mediterranean
shrublands, warming and drought have changed some
soil enzyme activities related to P turnover in some sea-
sons of a year (Sardans et al., 2006), while in Mediter-
ranean forests, urease, protease, and -glucosidase ac-
tivities decreased in spring and autumn in some cases
(Sardans and Penuelas, 2005).
Rhizodeposition consists of a continuous ow of
C-containing compounds from roots to soil. Simple
molecules such as sugars, amino acids, sugar alco-
hols, organic acids, and more structurally complex se-
condary metabolites are among the chemical groups
that make up a plethora of root exudates (Bais et
al., 2006) that can be rapidly (hours to days) respired
following their deposition to soil (Muller et al., 1993).
However, polymers (lignin, cellulose, and hemicellulo-
ses) requires extracellular enzymes for depolymeriza-
tion before they can be taken into the microbial cell
and metabolized (Kogel-Knabner, 2002). The decom-
position kinetics of these complex molecules is acceler-
ated to a greater extent in anticipated global warming.
This review aims to ll the knowledge gap how soil
microbes respond to changing climatic variables, their
consequent eects on soil C sequestration, terrestrial C
cycle climate feedbacks, and novel techniques like omic
technological interventions to determine soil microbial
community shifts at taxa level.
MICROBIAL ACTIVITY AND C DYNAMICS
Soil microbial activities are of signicant impor-
tance in dening the ecosystem properties; under-
standing how soil microbe-microbe and soil microbe-
plant interactions respond to climate change is a rese-
SOIL MICROBIOLOGICAL ACTIVITY AND C DYNAMICS
arch priority that will shed light on important eco-
system functions such as soil C storage and net pri-
mary productivity (Berg et al., 2010; Fischer et al.,
2014). Soils, in combination with plant biomass, hold
nearly 2.5 times more C than the atmosphere (Singh
et al., 2010). Soils have the capacity to retain large
amounts of C and their ability to sequester C has
helped to mitigate rising atmospheric CO2 .
Several factors regulate the amount of C that soils
can sequester, including climate, soil parent material,
age, and texture, topography, vegetation type, and soil
community composition (Jenny, 1941). However, mi-
crobial decomposers ultimately regulate the rate-limi-
ting steps in the decomposition process and thus the
inuence of abiotic factors on decomposition. Yet, how
microbial activity will inuence C feedbacks among
plant, soil, and the atmosphere is uncertain (Treseder
et al., 2012; Verheijen et al., 2015). If the activity of
the soil community, such as the decomposition rate,
increases relative to inputs from plants and animals,
then the amount of C in soil will decrease as C enters
the atmosphere, which can amplify C climate feedbacks
(Zhou et al., 2009; Wieder et al., 2013).
Microbial activity and high temperature regime
One of the major uncertainties in climate change
prediction is the response of soil respiration to incre-
ased atmospheric temperatures (Briones et al., 2004).
Several studies have shown that increased tempe-
ratures accelerate microbial decomposition, thereby
increasing CO2 emitted by soil respiration and produ-
cing a positive feedback to global warming (Hawkes et
al., 2008; Malcolm et al., 2008; Allison et al., 2010a,
b; Vargas et al., 2010). The eects of increased global
temperature on soil are especially alarming when con-
sidering the eect that it has already begun to have
on one of the most important terrestrial C sinks, per-
mafrost. Permafrost is permanently frozen soil that
stores signicant amounts of C and organic matter in
its frozen layers. As permafrost thaws, the stored C
and organic nutrients become available for microbial
decomposition, which in turn releases CO2 into the at-
mosphere and causes a positive feedback to warming
(Davidson and Janssens, 2006). It is estimated that
25% of permafrost could thaw by 2100 as a result of
global warming, making about 100 Pg of C available
for microbial decomposition (Davidson and Janssens,
2006; Anisimov et al., 1999). However, further studies
suggest that this increase in respiration may not persist
as temperatures continue to rise.
In a 10-year soil warming experiment, the CO2 ux
increased by 28% in the rst 6 years of warming when
579
compared to the control soils, followed by considera-
ble decreases in CO2 released in subsequent years, and
no signicant response to warming in the nal year
of the experiment (Melillo et al., 2002). Contrarily,
many modeling experiments suggest that the results of
short-term soil warming are compatible with long-term
sensitivity of soil organic C (SOC) turnover (Knorr et
al., 2005). These experiments refute the claim that
increased SOC turnover is only a transient process,
which returns to pre-warming conditions after few
years, due to acclimation (French et al., 2009). More
long-term and large-scale eld-based studies are nee-
ded to better understand the relationship between ris-
ing atmospheric temperature and microbial activity in
soil.
Microbial activity and elevated CO2
It is well established that elevated CO2 increa-
ses plant photosynthesis and growth, especially under
nutrient-rich conditions (Curtis and Wang, 1998), and
this in turn increases the ux of C to roots, their sym-
bionts, and heterotrophic microbes through root exu-
dation of easily degradable sugars, organic acids, and
amino acids (Zak et al., 1993). The consequences of in-
creased C ux from roots to soil for microbial commu-
nities and C exchange are dicult to predict, because
they will vary substantially with factors such as plant
identity, soil food web interactions, soil fertility, and
a range of other ecosystem properties (Wardle, 2002;
Bardgett, 2005).
However, there are some potential outcomes for soil
microbes and C exchange, including i) increase in mi-
crobial activity in response to global warming which
leads to increase in soil respiration and hence C loss
and subsequently its eux to drainage and further in-
crease in N mineralization of recent and old soil orga-
nic C (Blagodatskaya and Kuzyakov, 2008; Langley
et al., 2009; Zhu and Cheng, 2011; Schleppi et al.,
2012), a phenomenon known as priming (Fontaine
and Barot, 2005; Kuzyakov, 2006; Dijkstra and Cheng,
2007), ii) enhanced microbial activity which may lead
to immobilization of N, thereby limiting N availability
to plants and creating a negative feedback that con-
strains future increases in plant growth and C transfer
to soil (Ainsworth and Long, 2005; Friedlingstein et al.,
2006), iii) increase in plant-microbe competition for N
which may lead to suppressed microbial decomposi-
tion and thus increased soil C accumulation (Hogberg
and Read, 2006), as well as selection for benecial fun-
gal strains that help their host plant meet increasing
nutrient demands (Gamper et al., 2005), leading to a
possible positive feedback of plant growth and C as-
580
similation and enhanced stabilization of soil organic
C through promotion of soil aggregation (Rillig and
Mummey, 2006; Sixet al., 2006), and iv) changes in rhi-
zodepsition in present global warming scenarios which
potentially enhance methanogenesis and hence C loss,
for which the mechanism is poorly understood (Strom
et al., 2005).
Further elevated CO2 levels can cause alteration
in the whole soil ecosystem. For instance, fungi might
come to dominate over bacteria, bacterial nutrition
groups may change, and mycorrhizal fungi can be
altered (Castro et al., 2010). Structural changes, in
turn, may have signicant eects on the functioning
(including emission of GHGs and nutrient cycling) of
the soil microbial community and its interaction with
the plant community (Bardgett et al., 2008; Drigo et
al., 2008). Elevated atmospheric CO2 may aect the
microbe-soil-plant root system indirectly by modifying
soil water content and by increasing root growth and
rhizodeposition rates. Therefore, changes in microbial
population, community structure, and activity of soil
and rhizosphere-associated microorganisms are likely
to occur under elevated CO2 .
Understanding how the balance between terrestri-
al ecosystem sinks (i.e., photosynthesis) and sources
(i.e., respiration, including microbial respiration) of
atmospheric CO2 will be aected in an elevated CO2
world is still one of the main uncertainties in under-
standing the coupled C-climate system (Hawkes et al.,
2008; Smith and Fang, 2010). Some modeling studies
have suggested that there may be a point during this
century where terrestrial ecosystems shift from a net
sink to a net source of atmospheric CO2 (Denman et
al., 2007), possibly reecting the scenarios of increased
microbial respiration (Bardgett et al., 2008). However,
these models are still at an early stage of development
(Friedlingstein et al., 2006). There exists a paucity of
data on eect of rising CO2 levels on soil microbes,
which prevents the concerned stakeholders to reach a
rm conclusion. Therefore, it is recommended that a-
long with large-scale eld experiments, microcosm stu-
dies may be undertaken in order to develop a thorough
understanding of how the rising CO2 levels can af-
fect soil geochemical parameters and the subsequent
response of the soil microbial community.
Microbial activity and soil moisture
Climate change is characterized by erratic precipi-
tation which may result in moisture decit or surplus,
a condition which can have direct or indirect eect
on microbial activities. Orchard and Cook (1983) ob-
served that a decrease in water potential from 0.01 to
J. A. SOFI et al.
0.02 MPa caused a 10% decrease in microbial activi-
ty. Rewetting the soil caused a large and rapid increase
in the respiration rate. Under drier conditions, micro-
organisms create high internal solute concentrations ei-
ther by producing compatible organic solutes or by ta-
king up ions from the extracellular solution (Csonka,
1989). High intracellular solute concentrations inhibit
enzyme activity because the resulting low water po-
tential reduces the degree of hydration of enzymes,
which may change enzyme conformation (Skujins and
McLaren, 1967; Lanyi et al., 1979; Csonka, 1989).
Total microbial biomass in the forest oor corre-
lates well with soil moisture (Wagener and Schimel,
1998) and soil drying limits microbial activity even in
winter when soil is frozen (Clein and Schimel, 1995).
The eects of drought and rewetting on total micro-
bial biomass and activity have been studied, but the
eects on microbial community structure are poor-
ly understood. Physiological stress, such as drought,
tends to reduce microbial diversity, favoring those mi-
crobes best adapted to coping with the stress (Atlas,
1984). Drought impacts ecosystem functions and plant-
microbe relationships in terrestrial environments (Grif-
ths et al., 2003; Solomon et al., 2007); it also aects
the partitioning of C between the atmosphere and ter-
restrial systems. For example, prolonged drought in
North America in 2002 reduced the amount of C up-
take by vegetation and soil from an annual average
of 650 to 330 Mt (Peters et al., 2007). Since the fre-
quency of heat and drought stresses is predicted to in-
crease (Mearns et al., 1984), it follows that the amount
of C sequestered by terrestrial ecosystems will likely
decrease. Consequently, the combination of increased
drought and CO2 enrichment could result in a chronic
impact on soil microbial communities and their rela-
tionships with plants. Drought threat has signicant
consequences for belowground C and nutrient cycling
(Raich and Schlesinger, 1992) and thus signicantly
aects microbial activity in soil. Moreover, the long
period of drought has negative impacts on uctuations
of soil moisture.
The issue of extreme uctuations of soil moisture
aects activity of soil microorganisms and their inu-
ence on soil hydrophobicity (Buzcko et al., 2005; Dia-
mantis et al., 2013; Doerr et al., 2000). Soil water
repellency (soil hydrophobicity) is a widespread phe-
nomenon, which aects inltration as well as soil wa-
ter retention and plant growth. It can be responsible
for enhanced surface runo, erosion, and preferential
ow. There is a complex of interactions between i) the
formation of hydrophobic lms on soil particles, ii) re-
duction of microbial activity, iii) leaching of nutrients
SOIL MICROBIOLOGICAL ACTIVITY AND C DYNAMICS
from the soil sorption complex, iv) stability of soil ag-
gregate, and v) content of water in soil (Doerr et al.,
2000; Cosentino et al., 2010; Diamantis et al., 2013).
Climate-related events like drought and freezing
have greater eect on microbial physiology than tem-
perature and precipitation, with important conseque-
nces for ecosystem-level C and nutrient ows (Schimel
et al., 2007). Drier soil moisture condition will result
in lesser microbial activity as reected in forest ecosys-
tem with signicant fall in litter phenol oxidase ac-
tivity and isoenzyme diversity, and soil bacterial and
fungal biomass during dry periods (Nardo et al., 2004;
Krivtsov et al., 2006). In contrast, increased drought
and drying in wetlands and peatlands will create more
favourable conditions for microbial activity, by lower-
ing the watertable and introducing oxygen into pre-
viously anaerobic soil as phenol oxidase activity was
found to be increased (Freeman et al., 2004; Zibilske
and Bradford, 2007), which play a pivotal role in the
breakdown of complex organic matter and the cycling
of phenolic compounds that may interfere with extra-
cellular enzymes (Benoit and Starkey, 1968; Albers
et al., 2004). Peat-lands and wetlands are one of the
largest stocks of terrestrial carbon (Ward et al., 2007),
such enhanced breakdown of recalcitrant organic ma-
tter under drying could have major implications for the
global carbon cycle (Freeman et al., 2004).
Extracellular enzyme activity and climate change
Soil temperature and moisture changes due to cli-
mate change will aect enzyme activities in com-
plex ways that are dicult to predict (Burns et al.,
2013). For instance, extracellular enzyme activity
(EAA) increases with increase in temperature till its
optimum is reached and thus climate warming may
increase the rate of enzymatically catalyzed reactions
(Wallenstein and Weintraub, 2008). Contrastingly, mi-
crobes may decrease enzyme synthesis and secretion in
response to warming (Wallenstein et al., 2012; Burns
et al., 2013). Mass ow models of C often assume that
C ow is linked to warming via both temperature-
dependent microbial activity, which drives enzyme pro-
duction, and the direct temperature dependence of en-
zyme activity in the soil, as inferred in a warming ex-
periment (Bengtson and Bengtsson, 2007); however,
microbial activity can also decrease in response to war-
ming when warming decreases soil moisture (Allison
and Treseder, 2008). Additionally, enzyme denatura-
tion rates and the degradative activity of extracellular
protease could also upsurge with warming (Wallenstein
et al., 2012), which would oset any changes in enzyme
pool sizes. Explicitly, it is more onerous to make gene-
581
ralizations with regard to the eects of warming on
enzyme pools. Frequent drying of soils due to climate
change introduces both matric and osmotic stresses
which in turn aect enzyme activities as microbes focus
on intracellular maintenance strategies like synthesi-
zing osmolytes (Schimel et al., 2007; Chowdhury et al.,
2011).
The response of extracellular enzyme activity to
global warming measured using various experimental
techniques, such as open top chambers, greenhouses,
retractable passive warming curtains, snow removal,
heated coils/uid lled tubes inserted into soil, or over-
head infrared heaters (Shen and Harte, 2000), have not
provided the real picture and can not trade o the in-
teractive components under natural conditions. In eld
experiments, the potential activities of both hydro-
lase and oxidative enzymes often have not responded
signicantly to warming treatments, as observed in a
Mediterranean shrubland (Sardans et al., 2007), an an-
nual grassland (Gutknecht et al., 2010), and temperate
old elds (Bell et al., 2010; Kardol et al., 2010) (Ta-
ble I). There is the potential for climate change eects
to interact with seasonal and inter-annual variations
in EEA. For example, in a rainfall and runo exclu-
sion experiment in a Mediterranean forest, treatment
effects on acid phosphatase activity were signicant
over autumn, winter, and spring, but not over sum-
mer (Sardans et al., 2008). Similarly, eects of other
few signicant interactions, such as those of CO2 and
N additions with warming or precipitation, on the po-
tential activities of hydrolytic and oxidative enzymes
exist despite the signicance of the main eects (Henry
et al., 2005; Menge and Field, 2007).
MICROBIAL ACTIVITY, GHG RELEASE AND C
SEQUESTRATION
Microbial activity and C exchange
Due to the temperature sensitivity of C cycling
processes, small changes in temperature could result
in a large release of soil C back to the atmosphere
(Classen et al., 2015). Besides, the most prominent di-
rect climate-microbe feedback mechanism is enhanced
organic matter decomposition by accelerating hete-
rotrophic microbes. As a result, there will be eux of
CO2 to atmosphere and export of dissolved organic C
to hydrologic leaching (Jenkinson et al., 1991; David-
son and Janssens, 2006). Soil respiration is more sen-
sitive than primary production (Schimel et al., 1994),
and hence it is anticipated that there will be more ef-
ux of CO2 to atmosphere, thus creating positive feed-
back on climate change (Cox et al., 2000). No relation-
582
TABLE I
Responses of extracellular enzyme activity (EEA) to climate change in eld experiments
Ecosystem Treatment
Mediterranean oak forest Runo and rainfall exclusion
Temperate old eld Open top chambers
Mediterranean shrubland Retractable rain curtains
Upland heathland Retractable rain curtains
Moist lowland tropical Water addition during
forest drought
Annual grassland Water addition
Temperate grassland and Rainout shelters, water
heath
Annual grassland Water addition
a) AG = -glucosidase; BG = -glucosidase; BX = -xylosidase; CBH = cellobiohydrolase; NAG = N -acetylglucosaminidase; PO =
peroxidase; PPO = polyphenol oxidase; PR = protease; PT = phosphatase; ST = sulphatase; UR = urease.
b) + indicates decreased activity; indicates increased activity; 0 indicates no change in activity.
ship has been established so far between temperature
and soil heterotrophic respiration and its feedback on
climate change (Trumbore, 2006) due to complexity
and diversity of soil organic matter (Davidson and
Janssens, 2006). However, models representing logi-
cal syntheses of assumptions and boundary conditions
can identify gaps in understanding and are useful for
revealing amplication and dampening eects (Raich,
2000). The development of methods to quantify micro-
bial impacts on climate so that they can be incorpo-
rated into climate models is a major interdisciplinary
challenge. Despite the important role of soil microbes
in the C cycle and the environmental implications of C
cycle-climate change feedbacks, most C cycle models
treat the soil microbial biomass as a black box (Ostle
et al., 2009).
Plant-derived C inputs strongly mediate the tem-
perature sensitivity of soil C decomposition, but the
relative importance of direct versus indirect eects of
climate change on soil C dynamics remains unresolved
especially in ecosystems that are in transition from one
state to another. Classen et al. (2015) opine that the
indirect eects of climate change on microbes media-
ted through plants may be stronger than direct eects
of climate on shaping of microbial community compo-
sition and function. Nevertheless, these eects need to
be measured at suitable temporal and spatial scales,
ideally in microbe-centric studies in order to comple-
ment the existing landscape of plant-centric climate
change studies. Novel technological approaches will be
vital in microbe-centric studies that aim to reveal those
taxa most sensitive to climate and those whose re-
J. A. SOFI et al.
Enzyme(s)a) examined Reference
(activity responseb) )
BG (+), PR (+), PT (+), UR (+) Sardans and Penuelas (2005)
AG (0), BG (0), BX (0), CBH (0), Kardol et al. (2010)
NAG (0), PO (0), PPO (0), PT (+),
ST (+)
PT (+) in rhizosphere Sardans et al. (2007)
PPO (+) Toberman et al. (2008)
PT (0), ST (0) Yavitt et al. (2004)
AG (+), BG (+), BX (+), CBH (+), Henry et al. (2005)
NAG (+), PO (0), PPO (0), PT (0)
BG (0), BX (+), CBH (+), NAG with Kreyling et al. (2008)
water addition (), PT (0)
AG (+), BG (0), BX (+), CBH (+), Gutknecht et al. (2010)
NAG (+), PT (0)
sponses lead to shifts in microbial community function.
Overall, these advances will be critical for making pre-
dictions about ecosystem tipping points, eects of ex-
treme events, and the stability of communities under
climate change.
Microbial activity and GHG emission
Globally soils are estimated to contain twice as
much C as the atmosphere, making them one of the
largest sinks for atmospheric CO2 and organic C (Wil-
ley et al., 2009). Much of this C is stored in wetlands,
peatlands, and permafrost, where microbial decompo-
sition of C is limited. The amount of C stored in the
soil is dependent on the balance between C inputs from
leaf litter and root detritus and C outputs from micro-
bial respiration underground (Davidson and Janssens,
2006).
Soil respiration refers to the overall process by
which bacteria and fungi in the soil decompose C and
release it into the atmosphere in the form of CO2 . This
process accounts for 25% of naturally emitted CO2 ,
which is the most abundant GHG in the atmosphere
and the target of many climate change mitigation ef-
forts. Small changes in decomposition rates could not
only aect CO2 emissions in the atmosphere, but may
also result in greater changes to the amount of C sto-
red in the soil over decades (Davidson and Janssens,
2006).
Methane formation under anaerobic condition by
microorganisms has signicant implications on global
warming potential as global warming potential of CH4
SOIL MICROBIOLOGICAL ACTIVITY AND C DYNAMICS
is signicantly higher than CO2 and it is imperative
to understand the methane formation, providing deep
insight for its possible coupling with some mechanistic
models (Fig. 1). Methane, an important GHG, is 25
times more eective than CO2 at trapping heat radi-
ated from the Earth (Schlesinger and Andrews, 2000).
Microbial methanogenesis is responsible for both na-
tural and human-induced CH4 emissions since metha-
nogenic archaea reduce C into methane in anaerobic,
C-rich environments such as ruminant livestock, rice
paddies, landlls, and wetlands. Not all of the methane
produced ends up in the atmosphere; methanotrophic
bacteria can oxidize methane into CO2 in the pres-
ence of oxygen (O2 ). When methanogens in the soil
produce methane faster than can be used by methano-
trophs in higher up oxic soil layers, methane escapes
into the atmosphere (Willey et al., 2009). Methano-
trophs are therefore important regulators of methane
uxes in the atmosphere, but their slow growth rate
and rm attachment to soil particles make them di-
cult to isolate. Further exploration of these methano-
trophs nature could potentially help reduce methane
emissions if they can be added to the topsoil of land-
lls, for example, and capture some of the methane
that would normally be released into the atmosphere.
Methanogenic pathways are negated by increasing
O2 under drought condition in wetlands and peat-
lands, thereby increasing CO2 release as compared to
methane. Watertable depth is a strong predictor of
methane emissions (Roulet and Moore, 1995), which
is generally assumed to be due to toxic eects of O2 ;
there is also evidence that methanogens are more sen-
sitive to desiccation (Fetzer et al., 1993). Toxic ee-
Fig. 1 Exchange of CO2 and CH4 between soil and atmosphere.
583
cts on methanogens of oxidized products of denitrica-
tion have also been noted (Kluber and Conrad, 1998),
and net methane emissions are also suppressed under
drought conditions by the action of methanotrophic
bacteria (King, 1992; Freeman et al., 2002).
Microbial processes are often dependent on envi-
ronmental factors such as temperature, moisture, en-
zyme activity, and nutrient availability, all of which are
likely to be aected by climate change (Solomon et al.,
2007). These changes may have greater implications
for crucial ecological processes such as nutrient cycling,
which rely on microbial activity. For example, soil res-
piration is dependent on soil temperature and moisture
and may increase or decrease as a result of changes in
precipitation and increased atmospheric temperatures.
Due to its importance in the global C cycle, changes
in soil respiration may have signicant feedback ee-
cts on climate change and severely alter aboveground
communities. Thus, understanding the response of soil
respiration to climate change is of utmost importance
and the need of the hour to ponder upon.
Microbial activity and C sequestration
The equilibrium among organic matter inputs and
losses (respiration and decomposition) determines soil
C levels. Organic C taken up by the microorganisms
is segregated between biomass production and respira-
tion. The microbial C input to the soil depends on the
microbial growth eciency (MGE), degree of protec-
tion of microbial biomass in the soil, and the degree at
which microbial derivatives are decomposed by other
microorganisms (Six et al., 2006). The lower the MGE
584
and degree of protection of the microbial biomass,
the more the microbial organic matter C is lost as
CO2 . Fungal cell walls contain polymers of melanin
and chitin which are resistant to degradation, whereas
phospholipids, main components of bacterial cell wall
membrane, are energy-rich, readily decomposable sub-
strates available to a wide range of soil microorganisms.
The storage of C is expected to be more persis-
tent when mediated by fungal biomass and more la-
bile when mediated by bacterial biomass (Bailey et al.,
2002). The extent to which climatic eects on soil C
cycling are confounded with microbial adaptation to
certain environmental niches is currently unknown. As
reviewed by Six et al. (2006), there is evidence sugges-
ting that the relative abundance of fungi and bacteria
may be important, with more stable C being formed
in soils with high fungal/bacterial biomass ratios. The
fungi have a higher C use eciency than bacteria and
therefore form more biomass per unit of C utilized
and also have a biomass (subsequently necromass) of
a more recalcitrant nature, which are two suggested
mechanisms for their greater accumulation of soil orga-
nic matter (SOM) and require further studies (Six et
al., 2006). Thus, the ecosystems with fungal-dominated
soil communities may have higher C retention than soil
communities dominated by bacteria (Six et al., 2006;
Clemmensen et al., 2013; Grover et al., 2015). There
have also been some studies reviewed in Nielsen et al.
(2011) that have reported relationships (positive and
negative) between soil biodiversity and C cycling pro-
cesses such as respiration, but these studies have gene-
rally focused on total species richness as the biodiver-
sity measure and not the richness or identity of those
species processing C in situ. The fate of C in the soil
is aected by diversity of microbial population and the
edaphic abiotic factors controlling microbial C utiliza-
tion eciency have not been thoroughly characterized
(Cotrufo et al., 2013). It is not clear to what extent
rhizosphere microbes within agricultural systems can
be manipulated for C sequestration.
It is estimated that 4278 Gt of C (Lal, 2004) that
was historically stored in the soil system has been lost
as a result of the intensive cultivation of soils, and
the capacity for agricultural soils to regain this lost
C is currently being discussed as one potential contri-
bution to atmospheric C remediation and mitigation
of climate change (Lal, 2004; Smith and Olsen, 2010).
Strategies with respect to the management of soil for C
sequestration therefore involve increasing the quantity
of primary production and indeed other organic inputs
into the system. A second strategy involves manipu-
lating the fate of the inputs added to the soil. Inputs
J. A. SOFI et al.
once added to the soil may (after extracellular depoly-
merisation in the case of macromolecular constituents)
be taken up by the soil microorganisms and the C ta-
ken up by soil microbes may be partitioned for use in
the production of biomass (subsequently necromass),
excretions and secretions (e.g., extracellular enzymes)
and respiration. The aim of this second strategy is to
encourage the processing of plant-derived C to biomass
and metabolite precursors of SOM or to secretions that
promote the physical protection of C substrates against
decomposition rather than to CO2 .
TOOLS FOR ASSESSING MICROBIAL IMPACT
UNDER CLIMATE CHANGE SCENARIOS
Many previous studies examining either the impact
of elevated atmospheric CO2 or N deposition on mi-
crobial community composition, biomass, and function
have produced mixed results. For instance, in response
to elevated CO2 , increases in fungal biomass, num-
ber of sporocarps, root tips (Treseder, 2004), colony-
forming units (CFU) (Olszyk et al., 2001), arbuscu-
lar mycorrhizal hyphae (Treseder et al., 2003), and
relative abundance have been noted in studies using
quantitative polymerase chain reaction (qPCR) and
Sanger sequencing (Lesaulnier et al., 2008; Castro
et al., 2010). However, contrasting results have been
found in surveys of fungal saprotrophs using exoen-
zyme activities and ribosomal RNA (rRNA) genes am-
plied from soil DNA (Moorhead and Linkins, 1997;
Larson et al., 2002; Janus et al., 2005; Chung et al.,
2006; Carneyet al., 2007; Lesaulnier et al., 2008; Kelley
et al., 2011). Fungal ribosomal gene surveys that ex-
amined responses to N fertilization have documented
increased abundances of Ascomycota in fertilized soils
(Nemergut et al., 2008). However, the feedback that
this phylum-level shift has on C cycling remains poorly
understood. The role of N in altering net primary pro-
ductivity can vary, depending on the amount of CO2
that is available to drive photosynthesis (McGuire et
al., 1995), which may dierentially impact the function
of soil fungal communities. As a consequence of these
mixed results, the impacts of simultaneous increases
in N deposition and atmospheric CO2 levels on C se-
questration and microbial feedbacks remain dicult to
predict.
Traditionally, studies aiming at understanding mi-
crobial dynamics have used methods such as phospho-
lipid fatty acid analysis (PLFA), terminal restriction
fragment length polymorphism (TRFLP), denaturing
gel gradient electrophoresis (DGGE), or simply mea-
sures of biomass to understand complex community
SOIL MICROBIOLOGICAL ACTIVITY AND C DYNAMICS
dynamics and function. While these methods have ex-
posed patterns of microbial community composition at
a coarse level (Gray et al., 2011), they do not show in-
dividual taxa responses and give limited insight into
functional shifts. With the advent of new sequencing
technologies and in the wake of the omics revolution,
researchers have begun to explore microbial interac-
tions with hosts at a higher resolution and with more
functional signicance. By using metagenomics, meta-
transcriptomics, metaproteomics, and metabolomics,
scientists are able to dene changes in microbial com-
munities, which will result in a better understanding
of which microbes are present in an ecosystem and
what their potential functions are (Castro et al., 2012;
Muller et al., 2013). Furthermore, with technologies
such as stable isotope probing, it is possible to target
the active microbial community involved in a myriad
of functions (Mau et al., 2015).
The studies described above were DNA-based sur-
veys of r-RNA gene fragments. Because all organisms
contain ribosomal genes and cellulose-degrading mi-
croorganisms are not phylogenetically cohesive, riboso-
mal gene surveys are unable to detect specic respons-
es of cellulolytic microorganisms that may be central
in altered soil C cycling patterns. Furthermore, DNA-
based studies probe all members of the community
whether or not they are actively participating at the
time of sampling. The recent design of PCR primers
that target the gene coding for the catalytic subunit
of fungal glycosyl hydrolase family cellobiohydrolase I
(cbhI), a key enzyme involved in cellulose degradation,
has enabled monitoring eorts of a subset of celluloly-
tic soil fungi using DNA- and RNA-based approaches
(Edwards et al., 2008). In a comparison of DNA- and
RNA-based compositional surveys of cbhI in litter and
soil, Baldrian et al. (2011) demonstrated that some
of the most abundant taxa in the DNA-based surveys
did not dominate gene expression at the same time.
This brings into question the functional importance of
the most abundant taxa and provides a rationale for
using both DNA- and RNA-based, functional gene ap-
proaches to examine functional group and individual
taxon responses to environmental perturbations.
In an experiment which included frequent freeze-
thaw cycles (FTC) at Antarctic soils, Yergeau and
Kowalchuk (2008) assessed bacterial and fungal den-
sity and community structure, as well as the density
of several key genes in microbial nutrient cycles using
a combination of RNA- and DNA-based molecular n-
gerprinting and quantitative PCR approaches in addi-
tion to enzymatic activity assays. Their results showed
that bacteria were more aected by warming than by
585
changes in FTC frequency. In contrast, fungal commu-
nity structure and abundance were mostly inuenced
by FTC frequency, as well as the presence of vegeta-
tion cover. The relative densities of several bacterial
gene families involved in key steps of the N cycle were
aected by FTC, while warming had little or no eect.
FUTURE CHALLENGES IN MICROBIAL ACTIVI-
TY AND C DYNAMICS VIS-A-VIS CLIMATE CHA-
NGE
An understanding of soil microbial ecology is pivo-
tal to assess terrestrial C cycle climate feedbacks.
However, the intricacy of the soil microbial popula-
tion and its numerous roles, coupled with innumerable
ways that climate and other global changes can aect
soil microbes, makes it onerous to draw rm conclu-
sions from the above review. Despite this uncertainty,
we argue that progress can be made in understanding
the potential negative and positive contributions of soil
microbes to global warming through consideration of
both direct and indirect impacts of climate change on
microorganisms. This is a big challenge, but we held
that progress can be made through the use of long-term
factorial eld experiments in relevant biomes, which in-
corporate consideration of direct and indirect impacts
of climate change on soil microbes and their contri-
bution to land-atmosphere C exchange. Such studies
necessitate a collaborative approach to link microbial
ecology to ux measures at the whole ecosystem scale.
Yet it is at infancy stage and we have only touched
the surface of the contribution of soil microbes to cli-
mate change. Besides what is mentioned above, there
are many other challenges: i) there is an extreme di-
versity among soil microbial communities, ii) how this
diversity responds to climate change, and iii) the func-
tional consequences of this diversity for ecosystem C
exchange, including the uptake, stabilization and re-
lease of C from soil as GHG. In addition, uncultivable
nature of many microbes is a major hurdle as it be-
comes dicult to test how they respond to, or modi-
fy, their environment. Nevertheless, new molecular and
stable isotope probing tools are being developed, which
enable linking of uctuations in microbial diversity to
ecosystem function, by focusing on functional genes
that are vital for biogeochemical processes and through
directly labeling DNA, RNA, and PLFA of organi-
sms participating in specic pathways (Neufeld et al.,
2007). These tools have changed the way that microbial
ecologists unfold the ecophysiology of microbial popu-
lations in the natural environment because they enable
study of uncultivable microorganisms, thus providing
586
insights into the underlying processes regulating C ow
in through dierent components of the soil microora.
More importantly, soil microbes and their activities are
intimately linked to aboveground communities. Under-
standing the eects of climate change on C dynamics
therefore requires the obvious consideration of the in-
teractions that occur between aboveground and be-
lowground communities and their responses to climate
change.
CONCLUSIONS
Soil microbes are the main drivers for the nutri-
ent cycling and C dynamics in a pedosystem, which
are the main determinants for soil quality. Altered soil
moisture and temperature regimes in present clima-
tic scenarios directly or indirectly aect soil microbes
which can have positive or negative feedback to climate
changes. Elevated CO2 signicantly aects photosyn-
thesis, which modies the rhizodeposition, soil C pools,
and nutrient dynamics, and subsequently alters micro-
bial activities. Soil enzyme activities are sensors of
soil microbial status and soil physico-chemical condi-
tions. Shifts in microbial community in response to cli-
mate change have been determined by gene probing,
PLFA, TRFLP, and DGGE, but in a recent investi-
gations, omic technological interventions have enabled
determination of the shift in soil microbe communi-
ty at a taxa level, which can provide very important
inputs for modeling C sequestration process. The in-
tricacy and diversity of the soil microbial population
and how it responds to climate change are big chal-
lenges, but new molecular and stable isotope probing
tools are being developed for linking uctuations in
microbial diversity to ecosystem function.
ACKNOWLEDGEMENT
The authors gratefully acknowledge the anonymous
reviewers for their constructive advice.
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