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      Modeling adaptation of carbon use efficiency in microbial communities

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          Abstract

          In new microbial-biogeochemical models, microbial carbon use efficiency (CUE) is often assumed to decline with increasing temperature. Under this assumption, soil carbon losses under warming are small because microbial biomass declines. Yet there is also empirical evidence that CUE may adapt (i.e., become less sensitive) to warming, thereby mitigating negative effects on microbial biomass. To analyze potential mechanisms of CUE adaptation, I used two theoretical models to implement a tradeoff between microbial uptake rate and CUE. This rate-yield tradeoff is based on thermodynamic principles and suggests that microbes with greater investment in resource acquisition should have lower CUE. Microbial communities or individuals could adapt to warming by reducing investment in enzymes and uptake machinery. Consistent with this idea, a simple analytical model predicted that adaptation can offset 50% of the warming-induced decline in CUE. To assess the ecosystem implications of the rate-yield tradeoff, I quantified CUE adaptation in a spatially-structured simulation model with 100 microbial taxa and 12 soil carbon substrates. This model predicted much lower CUE adaptation, likely due to additional physiological and ecological constraints on microbes. In particular, specific resource acquisition traits are needed to maintain stoichiometric balance, and taxa with high CUE and low enzyme investment rely on low-yield, high-enzyme neighbors to catalyze substrate degradation. In contrast to published microbial models, simulations with greater CUE adaptation also showed greater carbon storage under warming. This pattern occurred because microbial communities with stronger CUE adaptation produced fewer degradative enzymes, despite increases in biomass. Thus, the rate-yield tradeoff prevents CUE adaptation from driving ecosystem carbon loss under climate warming.

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          Most cited references40

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          Soil-carbon response to warming dependent on microbial physiology

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            Environmental and stoichiometric controls on microbial carbon-use efficiency in soils.

            Carbon (C) metabolism is at the core of ecosystem function. Decomposers play a critical role in this metabolism as they drive soil C cycle by mineralizing organic matter to CO(2). Their growth depends on the carbon-use efficiency (CUE), defined as the ratio of growth over C uptake. By definition, high CUE promotes growth and possibly C stabilization in soils, while low CUE favors respiration. Despite the importance of this variable, flexibility in CUE for terrestrial decomposers is still poorly characterized and is not represented in most biogeochemical models. Here, we synthesize the theoretical and empirical basis of changes in CUE across aquatic and terrestrial ecosystems, highlighting common patterns and hypothesizing changes in CUE under future climates. Both theoretical considerations and empirical evidence from aquatic organisms indicate that CUE decreases as temperature increases and nutrient availability decreases. More limited evidence shows a similar sensitivity of CUE to temperature and nutrient availability in terrestrial decomposers. Increasing CUE with improved nutrient availability might explain observed declines in respiration from fertilized stands, while decreased CUE with increasing temperature and plant C : N ratios might decrease soil C storage. Current biogeochemical models could be improved by accounting for these CUE responses along environmental and stoichiometric gradients. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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              Microbial contributions to climate change through carbon cycle feedbacks.

              There is considerable interest in understanding the biological mechanisms that regulate carbon exchanges between the land and atmosphere, and how these exchanges respond to climate change. An understanding of soil microbial ecology is central to our ability to assess terrestrial carbon cycle-climate feedbacks, but the complexity of the soil microbial community and the many ways that it can be affected by climate and other global changes hampers our ability to draw firm conclusions on this topic. In this paper, we argue that to understand the potential negative and positive contributions of soil microbes to land-atmosphere carbon exchange and global warming requires explicit consideration of both direct and indirect impacts of climate change on microorganisms. Moreover, we argue that this requires consideration of complex interactions and feedbacks that occur between microbes, plants and their physical environment in the context of climate change, and the influence of other global changes which have the capacity to amplify climate-driven effects on soil microbes. Overall, we emphasize the urgent need for greater understanding of how soil microbial ecology contributes to land-atmosphere carbon exchange in the context of climate change, and identify some challenges for the future. In particular, we highlight the need for a multifactor experimental approach to understand how soil microbes and their activities respond to climate change and consequences for carbon cycle feedbacks.
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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
                28 October 2014
                2014
                : 5
                : 571
                Affiliations
                [1] 1Department of Ecology and Evolutionary Biology, University of California Irvine Irvine, CA, USA
                [2] 2Department of Earth System Science, University of California Irvine Irvine, CA, USA
                Author notes

                Edited by: Peter Van Bodegom, VU University Amsterdam, Netherlands

                Reviewed by: Raffaella Balestrini, Consiglio Nazionale delle Ricerche, Italy; Aline Frossard, University of Pretoria, South Africa

                *Correspondence: Steven D. Allison, Department of Ecology and Evolutionary Biology, University of California Irvine, 321 Steinhaus, Irvine, CA 92697, USA e-mail: allisons@ 123456uci.edu

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

                Article
                10.3389/fmicb.2014.00571
                4211550
                24523715
                b39ab2f8-ad05-469a-92a7-947f0f48c13e
                Copyright © 2014 Allison.

                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
                : 30 June 2014
                : 09 October 2014
                Page count
                Figures: 4, Tables: 2, Equations: 7, References: 49, Pages: 9, Words: 6381
                Categories
                Microbiology
                Original Research Article

                Microbiology & Virology
                bacteria,climate change,fungi,rate-yield tradeoff,soil carbon,temperature,theoretical model

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