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Title: Modeling adaptation of carbon use efficiency in microbial communities

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 relymore » 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.« less

Authors:
 [1]
  1. Univ. of California, Irvine, CA (United States). Dept. of Ecology and Evolutionary Biology; Univ. of California, Irvine, CA (United States). Dept. of Earth Systems Science
Publication Date:
Research Org.:
Univ. of California, Irvine, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1628125
Grant/Contract Number:  
FG02-00ER41132
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; bacteria; climate change; fungi; rate-yield tradeoff; soil carbon; temperature; theoretical model

Citation Formats

Allison, Steven D. Modeling adaptation of carbon use efficiency in microbial communities. United States: N. p., 2014. Web. doi:10.3389/fmicb.2014.00571.
Allison, Steven D. Modeling adaptation of carbon use efficiency in microbial communities. United States. https://doi.org/10.3389/fmicb.2014.00571
Allison, Steven D. Tue . "Modeling adaptation of carbon use efficiency in microbial communities". United States. https://doi.org/10.3389/fmicb.2014.00571. https://www.osti.gov/servlets/purl/1628125.
@article{osti_1628125,
title = {Modeling adaptation of carbon use efficiency in microbial communities},
author = {Allison, Steven D.},
abstractNote = {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.},
doi = {10.3389/fmicb.2014.00571},
journal = {Frontiers in Microbiology},
number = ,
volume = 5,
place = {United States},
year = {Tue Oct 28 00:00:00 EDT 2014},
month = {Tue Oct 28 00:00:00 EDT 2014}
}

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Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique
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Patterns of substrate utilization during long-term incubations at different temperatures
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Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment
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Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities
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Cooperation, Competition, and Coalitions in Enzyme-Producing Microbes: Social Evolution and Nutrient Depolymerization Rates
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Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources
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Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
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