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      Changes in the Size of the Active Microbial Pool Explain Short-Term Soil Respiratory Responses to Temperature and Moisture

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          Abstract

          Heterotrophic respiration contributes a substantial fraction of the carbon flux from soil to atmosphere, and responds strongly to environmental conditions. However, the mechanisms through which short-term changes in environmental conditions affect microbial respiration still remain unclear. Microorganisms cope with adverse environmental conditions by transitioning into and out of dormancy, a state in which they minimize rates of metabolism and respiration. These transitions are poorly characterized in soil and are generally omitted from decomposition models. Most current approaches to model microbial control over soil CO 2 production relate responses to total microbial biomass (TMB) and do not differentiate between microorganisms in active and dormant physiological states. Indeed, few data for active microbial biomass (AMB) exist with which to compare model output. Here, we tested the hypothesis that differences in soil microbial respiration rates across various environmental conditions are more closely related to differences in AMB (e.g., due to activation of dormant microorganisms) than in TMB. We measured basal respiration (SBR) of soil incubated for a week at two temperatures (24 and 33°C) and two moisture levels (10 and 20% soil dry weight [SDW]), and then determined TMB, AMB, microbial specific growth rate, and the lag time before microbial growth ( t lag ) using the Substrate-Induced Growth Response (SIGR) method. As expected, SBR was more strongly correlated with AMB than with TMB. This relationship indicated that each g active biomass C contributed ~0.04 g CO 2-C h −1 of SBR. TMB responded very little to short-term changes in temperature and soil moisture and did not explain differences in SBR among the treatments. Maximum specific growth rate did not respond to environmental conditions, suggesting that the dominant microbial populations remained similar. However, warmer temperatures and increased soil moisture both reduced t lag , indicating that favorable abiotic conditions activated soil microorganisms. We conclude that soil respiratory responses to short-term changes in environmental conditions are better explained by changes in AMB than in TMB. These results suggest that decomposition models that explicitly represent microbial carbon pools should take into account the active microbial pool, and researchers should be cautious in comparing modeled microbial pool sizes with measurements of TMB.

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          Most cited references59

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          Soil-carbon response to warming dependent on microbial physiology

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            The effect of soil drying on humus decomposition and nitrogen availability

            H. Birch (1958)
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              Dormancy contributes to the maintenance of microbial diversity.

              Dormancy is a bet-hedging strategy used by a variety of organisms to overcome unfavorable environmental conditions. By entering a reversible state of low metabolic activity, dormant individuals become members of a seed bank, which can determine community dynamics in future generations. Although microbiologists have documented dormancy in both clinical and natural settings, the importance of seed banks for the diversity and functioning of microbial communities remains untested. Here, we develop a theoretical model demonstrating that microbial communities are structured by environmental cues that trigger dormancy. A molecular survey of lake ecosystems revealed that dormancy plays a more important role in shaping bacterial communities than eukaryotic microbial communities. The proportion of dormant bacteria was relatively low in productive ecosystems but accounted for up to 40% of taxon richness in nutrient-poor systems. Our simulations and empirical data suggest that regional environmental cues and dormancy synchronize the composition of active communities across the landscape while decoupling active microbes from the total community at local scales. Furthermore, we observed that rare bacterial taxa were disproportionately active relative to common bacterial taxa, suggesting that microbial rank-abundance curves are more dynamic than previously considered. We propose that repeated transitions to and from the seed bank may help maintain the high levels of microbial biodiversity that are observed in nearly all ecosystems.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                19 April 2016
                2016
                : 7
                : 524
                Affiliations
                [1] 1Department of Biological Sciences, Purdue University West Lafayette, IN, USA
                [2] 2Purdue Climate Change Research Center, Purdue University West Lafayette, IN, USA
                [3] 3Department of Soil Science of Temperate Ecosystems, University of Göttingen Göttingen, Germany
                [4] 4Department of Soil C and N Cycles, Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences Pushchino, Russia
                [5] 5Department of Forestry and Natural Resources, Purdue University West Lafayette, IN, USA
                Author notes

                Edited by: Jay T. Lennon, Indiana University, USA

                Reviewed by: Emma L. Aronson, University of California, Riverside, USA; Melany Fisk, Miami University, USA

                *Correspondence: Alejandro Salazar-Villegas alejandro.salazar-villegas@ 123456fulbrightmail.org

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.00524
                4836035
                27148213
                482161a8-d654-4d3d-9d00-8f3370617afa
                Copyright © 2016 Salazar-Villegas, Blagodatskaya and Dukes.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 20 December 2015
                : 30 March 2016
                Page count
                Figures: 6, Tables: 0, Equations: 6, References: 71, Pages: 10, Words: 7860
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                soil respiration,microbial dormancy,microbial biomass,substrate-induced growth response,carbon pool

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