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Science of the Total Environment 634 (2018) 497–500

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Short Communication

Soil microbial biomass: A key soil driver in management of


ecosystem functioning
Jay Shankar Singh a,⁎, Vijai Kumar Gupta b
a
Department of Environmental Microbiology, Babasaheb Bhimrao Ambedkar (Central) University, Raebarelly Road, Lucknow 226025, Uttar Pradesh, India
b
Department of Chemistry and Biotechnology, ERA Chair of Green Chemistry, School of Science, Tallinn University of Technology, Akadeemia tee 15, 12618 Tallinn, Estonia

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Soil microbial biomass as a key ecologi-


cal driver has been described.
• Soil microbial diversity and biomass
play key roles in the ecosystem services.
• Soil micro-flora N uptake is an adapta-
tion for short-term storage of N in ter-
restrial ecosystems.
• Soil microbial biomass is key ecological
driver in rehabilitation of degraded
lands.

a r t i c l e i n f o a b s t r a c t

Article history: Although patterns of microbial diversity and biomass have been described and reviewed at local and regional
Received 28 February 2018 scales, a unifying driver, or set of environmental drivers affecting soil microbial biomass (SMB) pattern at global
Received in revised form 30 March 2018 level is still missing. Biomass of soil microbial community, known as SMB is considered widely as the index of soil
Accepted 30 March 2018
fertility and ecosystem productivity. The escalating soil stresses due to land degradation and climatic variability
Available online 7 April 2018
are directly correlated with loss of microbial diversity and abundance or biomass dynamics. Therefore, alleviating
Editor: Frederic Coulon soil stresses on microbial communities with ecological restoration could reduce the unpredictability and turn-
over rates of SMB. Thus, the key ecological factors which stabilize the SMB and minimize its turnover, are sup-
Keywords: posed to play an important role in the soil nutrient dynamics and productivity of the ecosystems. Because of
Land degradation the existing public concern about the deleterious impacts of ecosystem degradation, there is an increasing inter-
Environmental drivers est in improving the understanding of SMB, and the way, it contributes to restoration and functioning of
Microbial community ecosystems.
Soil microbial biomass © 2018 Elsevier B.V. All rights reserved.

1. Microbial biomass under different ecological regimes and ecosys- microbial interactions in the soil-plant-animal food web (Seneviratne,
tem types 2015). Soil microbial diversity and abundance/biomass play key roles
in the ecosystem sustainability by maintaining essential functions of
Functioning of ecosystems rely on the flux of chemical signals, car- soil health, through carbon and nutrient turnover. Even after distur-
bon, and nutrients across the trophic levels, mainly mediated by bances, an ecosystem with a higher microbial diversity and biomass
may have a higher capacity to sustain the ecological processes through
⁎ Corresponding author. microbiological buffering. There is now increasing evidence that above-
E-mail address: jayshankar_1@yahoo.co.in (J.S. Singh). ground (plant litter quantity and quality) and belowground (soil

https://doi.org/10.1016/j.scitotenv.2018.03.373
0048-9697/© 2018 Elsevier B.V. All rights reserved.
498 J.S. Singh, V.K. Gupta / Science of the Total Environment 634 (2018) 497–500

microbial flora and fauna diversity) are key drivers that play fundamen- forests and mycorrhizae in boreal temperate forests) it is suggested
tal roles in controlling ecosystem processes and stability (Wardle et al., that variations in the size of SMB can impact to variability of the func-
2004). However, understanding ecological linkages between above- tioning of various ecosystem types.
and belowground abiotic and biotic (including SMB) attributes is still The rise in unpredictable climate shift and anthropogenic perturba-
a key challenge for our knowledge on the stability and functioning of tions are the critical drivers to regulate the existence and survival of in-
ecosystem processes. Therefore, given the importance of SMB dynamics digenous microbial diversity, and consequently, the essential soil
in defining ecosystem properties, the understanding as to how SMB re- functioning of the ecosystem. The macroclimate, topography and soil
spond to unexpected rise in biotic and abiotic drivers and loss of plant quality (pH, organic C and N, moisture, etc.) are the key drivers in con-
species diversity seems a research priority that would shed light on trolling SMB dynamics across different ecosystems and locations
the performance of diverse ecosystems. (Wardle, 1992). The temporal dynamics of SMB is likely to be the key
Among the various ecological drivers, microbes (N2-fixers, P- factor in determining the extent of release of immobilized labile nutri-
solubilizers, growth hormone producers, etc.) and their SMB pools ents due to microbial cell deaths, and the availability of nutrients re-
may be considered as major ecological impetus in controlling the di- leased crucial to plant growth and ecosystem functioning (Wardle,
verse ecosystem functions globally (Table 1). Soil carbon (C) and nitro- 1998). The factors that provide viability to the soil microbial community
gen (N) together with phosphorus (P) and soil pH are the key drivers therefore, are assumed to enhance soil nutrient conservation in the
that may limit the functioning of various nutrient deprived ecosystems form of higher SMB size owing to the reduced release of immobilized
(Bru et al., 2011; Carnicer et al., 2015). In strongly soil N deprived eco- nutrients. While studying the effect of climatic disturbances on ecosys-
systems such as Arctic and Alpine Tundra and Temperate forests, nutri- tem types, we may expect SMB to have lesser temporal variability
ents release after soil micro-flora (SMB) death has been pointed out as owing to lesser disturbances.
an important source of plant nutrient N (van der Heijden et al., 2008). Along a large geographical area, climate variability, land use types
So, it is suggested that uptake of N by soil micro-flora might be an adap- and the dominant vegetation composition might be the key factors for
tation that may have developed for short-term storage of N in several SMB variability across different ecosystem types. Differences in the
terrestrial ecosystems, thus reducing the loss of N from the soil of nutri- quantity and quality of substrate (organic C and N) inputs caused by
ent poor ecosystems. It is also important to mention here that the chem- varying plant residue types (litter and fine roots) and the associated nu-
ical composition of plant residues (litter and fine roots) from diverse trient specificity can be crucial drivers to influence the SMB across the
plant species in an ecosystem could be unpredictable and therefore, dif- ecosystem types. Thus, the higher SMB in soil of scrub stand than
ferent microbial communities might be evolved to decay and decom- other ecosystems might be attributed mainly to the greater availability
pose the variety of litter types. As many microbial communities have of organic matter via vegetation cover with giant plant species. How-
restricted bio-geographic distributions (N2-fixing rhizobia in tropical ever, in case the temporal data on SMB from different ecosystems across
the globe were quantitatively analyzed, more persistent and less dis-
turbed ecosystems had higher SMB values than the most disturbed
Table 1 one (Wardle, 1998), though the temporal variability of different ecosys-
Microbes as key ecological drivers regulating functioning of diverse ecosystems.
tem types was substantially comparable. This indicates that temporal
Source: van der Heijden et al. (2008) Ecol. Lett. 11: 296–310.
SMB variability is solely governed by the dominant vegetation and
Ecosystem type Microbes Microbial functions land use type, but the nutrient turnover along with other edaphic fac-
Tropical savannah, Symbiotic, free living and Support plant productivity tors can be more effective than those in regulating the temporal SMB
some grasslands and endophytic N-fixing by supplying different variability. However, it is suggested that shifts in plant species composi-
tropical forests bacteria limiting nutrients (N) to tion during land use change, can influence the microbial community
the plants.
Endophytes enhance
composition dynamics and SMB basically by changing soil organic nutri-
growth and competitive ent status (Zhang et al., 2016). But it is still unclear as to why SMB is not
ability of their host plants. so responsive to large-scale disturbance regimes, such as invasions of
Deserts and boreal N-fixing cyanobacteria Contribute to the N alien species into new territories, climate change due to atmospheric
forests economy of ecosystems via
CO2 elevation, greater soil nitrogen deposition and land use changes
N cycling and accumulation
under extremely limited (Wardle et al., 2004), and therefore, further studies in this regard, will
N2-fixation situations. enhance our understanding about temporal microbial community com-
Helps in degraded land positions and biomass variability.
restoration. Although nutrient status, seasonality, soil factors, temperature, and
Tropical, temperate and Arbuscular mycorrhizal Enhanced P uptake of host
boreal forests, (AM), Ectomycorrhizal plant species when plant
other factors, are important drivers to control functioning of dry tropical
grassland and (EM) and Ericoid productivity is strongly forest ecosystem, SMB could be one of the vital factors affecting produc-
savannah ecosystems mycorrhizal (ERM) fungi limited by P availability. tivity in the tropical dry deciduous forests, as observed in the Vindhyan
Provide resistance to plants plateau (Singh et al., 2010). In India, the previous investigations regard-
against diseases, drought
ing SMB across the tropical dry deciduous forest ecosystems have been
and other environmental
stresses in nutrient poor conducted by selecting only one or the other sites on a temporal scale,
and degraded ecosystems. and without deciphering differences in SMB status and its role in distri-
Natural ecosystems P-solubilizing bacteria May constitute up to 40% of bution and variations of the dominant vegetation composition. It may
the cultivable population of be hypothesized that alterations in soil properties due to land uses
soil bacteria.
However, significance of
and anthropogenic activities would correspond to differences in the
bacteria in natural SMB size and turnover rates and consequently, to loss of vegetation
ecosystems is still in cover and ecosystem productivity. However, the experimental evidence
enigma and further studied for such arguments is still warranted.
are still warranted.
In nutrient poor ecosystems, SMB acts as the major reservoir of avail-
Tropical forests Nitrifying and denitrifying Indirectly reduce plant
bacteria productivity because about able nutrients, and plays very crucial roles in the survival of plants
50% of available soil N is (Singh et al., 2016a, 2016b; Vimal et al., 2017). In the dry tropical decid-
lost from the ecosystem by uous forest ecosystem, nutrient withdrawal from the senescing leaves
nitrification and and its immobilization in the SMB has been considered as the nutrient
denitrification processes
conserving adaptations in response to nutrient paucity, and thus SMB
J.S. Singh, V.K. Gupta / Science of the Total Environment 634 (2018) 497–500 499

constitutes the key available nutrient source for the survival of plant SMB, an important driver of ecosystem functioning, may be consid-
communities (Singh et al., 2010; Singh, 2015a, 2015b). The conversion ered as the sensitive key biological indicator of perturbations owing to
of forest into cropland and savanna due to plant harvesting may result soil disturbances (Zornoza et al., 2009). Research practices on degraded
a significant alterations in the size of SMB. Since, plant diversity is a land restoration, have mainly focused on the aboveground features with
key driver in controlling SMB (Thakur et al., 2015); any alterations in lesser emphasis on the belowground soil microbial processes and the
the soil properties due to deforestation may have significant impact patterns of SMB, which could play a vital role in productivity of the de-
on SMB stability and its turnover rates. As plant biodiversity is projected rived ecosystems. The soil microbial properties between degraded and
to decline in response to global environmental change factors, we can restored lands have been compared (Bini et al., 2013; Singh, 2016),
also expect indirect effects of key environmental drivers on SMB status but the knowledge about key environmental drivers influencing the
via alterations in plant community compositions. The increasing de- patterns of SMB and microbial community structure during restoration,
mand of agricultural land accelerates deforestation and consequently is still limited. Therefore, the study of SMB patterns and its relationship
disturbances in SMB trends had been noted. Although deforestation is to climate and soil drivers can enhance our understanding in rehabilita-
a common practice for the generation of agricultural managed land- tion of land uses like vast waste lands (e.g. spoiled coal mine areas). It is
use systems, afforestation has become a much discussed topic in recent suggested that during restoration programs, the belowground microbial
years (Singh et al., 2010). Therefore, we suggest that long-term investi- activities and their biomass development and responses must be con-
gations should be conducted on the SMB patterns, a sensitive nutrient sidered in implementation. It is proposed that restoration practices
pool that may respond to plant diversity loss compared to other envi- with mixed plant species having high biomass producing potential,
ronmental drivers. can contribute to speedy recovery of lost microbial diversity and SMB
turnovers (Singh, 2013; Araujo et al., 2013; Singh, 2014). The fast recov-
ery of microbial communities and SMB size due to mixed plantations
2. Microbial biomass in restoration of degraded land soil cover (Lange et al., 2015) compared to the monoculture plantations
productivity can help in the returning of the huge bulk of diverse types of plant-
derived resources (leaf litter, fine root biomass, root exudates or
Restoration ecology, a somewhat new thrust research area, still rhizodeposits) and favorable soil conditions. In view of these, it is rec-
needs rigorous explorations to achieve satisfactory results (Calmon ommended that plant species having high biomass production effi-
et al., 2011). As the changing global climate is one of the major environ- ciency, and favoring the establishment of beneficial microbial
mental challenges today, there is an urgent need to restore the huge de- (mycorrhizae and nitrogen-fixers) associations, should preferably be
graded land area to make it cultivable for the overall sustainable agro- selected during restoration programs.
environmental development. Size of SMB can provide one of the most Speedy recovery of soil productivity on the deforested area can be
satisfactory estimates of the productivity of any restored degraded achieved by afforestation of mixed plantations in association with suit-
land (do Couto et al., 2016). A lower ratio of SMB to the total soil organic able bio-inoculants, which can be a good microbial “booster” to enhance
nutrients seems to indicate good strength of degraded land rehabilita- the SMB and ecosystem productivity (Fig. 1). The inoculation of suitable
tion. Consequently, the ratio of SMB to the total organic nutrients may bio-fertilizers along with mixed plantations, not only increases the pop-
be considered as a reliable parameter for the success of degraded land ulation of the microbial strains inoculated, but also enhances diversity
rehabilitation. The re-established SMB status and its dynamics under and abundance of microbes native to the soil, through dormancy break-
prevailing environmental drivers may provide valuable information ing of their quiescent viable spores developed in response to environ-
about the restoration progress and productivity potential of derived mental stresses (Seneviratne and Kulasooriya, 2013; Singh and Strong,
lands for agriculture purposes. 2016). Thus, a combination of mixed plantation, stress-tolerant bio-

Re-vegetation of degraded land

Degraded land Crop land Forest ecosystem


 Microbial flora
and fauna Nutrient
 Plant litters uptake by
 Root exudates plants and
Soil microbial biomass
& soil
Solubilization micro-flora
Dissolved organic matter
Decomposition
Available nutrients

Nutrient immobilization Mineralization

Fig. 1. Schematic representation showing contribution of soil microbial biomass as source of plant available nutrients to agro- and forest ecosystems.
500 J.S. Singh, V.K. Gupta / Science of the Total Environment 634 (2018) 497–500

inoculants, and organic amendments in restoration of the degraded Calmon, M., Brancalion, P.H.S., Paese, A., Aronson, J., Castro, P., Costa da Silva, S., Rodrigues,
R.R., 2011. Emerging threats and opportunities for biodiversity conservation and eco-
lands may offer a tripartite association to augment soil nutrient turn- logical restoration in the Atlantic forest of Brazil. Restor. Ecol. 19, 154–158.
overs and consequently to reinstate productivity of stressed ecosys- Carnicer, J., Sardans, J., Stefanescu, C., Ubachd, A., Bartrons, M., Asensio, D., Penuelas, J.,
tems. However, it should be kept in mind that addition of microbial 2015. Global biodiversity, stoichiometry and ecosystem function responses to
human-induced C–N–P imbalances. J. Plant Physiol. 172, 82–91.
inoculants into new territories may greatly affect soil plant-microbe in- do Couto, G.M., Eisenhauer, N., de Oliveira, E.B., Cesarz, S., Feliciano, A.L.P., Marangon, L.C.,
teractions, especially when the new microbial species has vastly differ- 2016. Response of soil microbial biomass and activity in early restored lands in the
ent physiological behaviours from the indigenous micro- flora. No northeastern Brazilian Atlantic Forest. Restor. Ecol. 24, 609–616.
van der Heijden, M.G.A., Bardgett, R.D., van Straalen, N.M., 2008. The unseen majority: soil
information is available on how addition of exotic soil microbial inocu- microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol.
lants in association with re-vegetation of degraded lands can influences Lett. 11, 296–310.
the exiting native soil micro-biota, although these effects should be Lange, M., Eisenhauer, N., Sierra, C.A., Bessler, H., Engels, C., Griffiths, R.I., Mellado-
Vazquez, P.G., Malik, A.A., Roy, J., Scheu, S., Steinbeiss, S., Thomson, B.C., Trumbore,
strongest when the alien microbial inoculants has functional attributes
S.E., Gleixner, G., 2015. Plant diversity increases soil microbial activity and soil carbon
that are not compatibles to the indigenous microbial species. In our storage. Nat. Commun. 6, 6707.
opinion, the future research on SMB turnovers as affected by the key Seneviratne, G., 2015. Signal transduction in edaphic ecosystems governs sustainability.
ecological drivers and its correlation with the ecosystem functioning Agric. Ecosyst. Environ. 210, 47–49.
Seneviratne, G., Kulasooriya, S.A., 2013. Reinstating soil microbial diversity in
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3. Conclusions Singh, J.S., 2014. Cyanobacteria: a vital bio-agent in eco-restoration of degraded lands and
sustainable agriculture. Clim. Change Environ. Sustain. 2, 133–137.
Singh, J.S., 2015a. Microbes: the chief ecological engineers in reinstating equilibrium in
Besides the importance of physico-chemical and biological processes
degraded ecosystems. Agric. Ecosyst. Environ. 203, 80–82.
to maintain soil health, SMB may be the ‘keystone’ biological driver of Singh, J.S., 2015b. Plant-microbe interactions: a viable tool for agricultural sustainability.
ecosystem functioning. Loss of beneficial microbial diversity and SMB Appl. Soil Ecol. 92, 45–46.
associated to land use changes and erratic climate shifts, are the major Singh, J.S., 2016. Microbes play major roles in ecosystem services. Clim. Change Environ.
Sustain. 3, 163–167.
reasons for deterioration of soil fertility and ecosystem productivity. Singh, J.S., Strong, P.J., 2016. Biologically derived fertilizer: a multifaceted bio-tool in
Therefore, researches related to plant-microbe-soil associations to com- methane mitigation. Ecotoxicol. Environ. Saf. 124, 67–276.
bat problems of soil degradation need to be performed in greater depth. Singh, J.S., Kashyap, A.K., Singh, D.P., 2010. Microbial biomass C, N and P in disturbed dry
tropical forest soils, India. Pedosphere 20 (6), 780–788.
Today, it is the utmost need to maintain soil health and productivity Singh, J.S., Abhilash, P.C., Gupta, V.K., 2016a. Agriculturally important microbes in sustain-
with emphasis on restoration of vast area of the degraded lands using able food production. Trends Biotechnol. 34, 773–775.
efficient biomass producing novel plant species and microbial inocu- Singh, J.S., Kumar, A., Rai, A.N., Singh, D.P., 2016b. Cyanobacteria: a precious bio-resource
in agriculture, ecosystem, and environmental sustainability. Front. Microbiol. 7, 529.
lants. Finally, SMB is concluded to be an important index for the soil Thakur, M.P., Milcu, A., Manning, P., Niklaus, P.A., Roscher, C., Power, S., Reich, P.B., Scheu,
health and environmental sustainability. S., Tilman, D., Ai, F., Guo, H., Ji, R., Pierce, S., Ramirez, N.G., Richter, A.N., Steinauer, K.,
Strecker, T., Vogel, A., Eisenhauer, N., 2015. Plant diversity drives soil microbial bio-
mass carbon in grasslands irrespective of global environmental change factors.
Acknowledgement Glob. Chang. Biol. 21, 4076–4085.
Vimal, S.R., Singh, J.S., Arora, N.K., Singh, S., 2017. Soil-plant-microbe interactions in
JSS is thankful to Head, Department of Environmental Microbiology, stressed agriculture management: a review. Pedosphere 27, 177–192.
Wardle, D.A., 1992. A comparative assessment of factors which influence microbial bio-
BBA University, Lucknow, India for providing all kind of supports and mass carbon and nitrogen levels in soils. Biol. Rev. 67, 321–358.
the infrastructure facilities. Wardle, D.A., 1998. Controls of temporal variability of the soil microbial biomass: a global-
scale synthesis. Soil Biol. Biochem. 30 (13), 1627–1637.
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H., Wall, D.H.,
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