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 »
- Authors:
-
- 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}
}
Works referenced in this record:
The maintenance energy of bacteria in growing cultures
journal, October 1965
- Pirt, S. J.
- Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 163, Issue 991, p. 224-231
Availability of public goods shapes the evolution of competing metabolic strategies
journal, August 2013
- Bachmann, H.; Fischlechner, M.; Rabbers, I.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 35
Global soil carbon projections are improved by modelling microbial processes
journal, July 2013
- Wieder, William R.; Bonan, Gordon B.; Allison, Steven D.
- Nature Climate Change, Vol. 3, Issue 10
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
journal, March 2006
- Davidson, Eric A.; Janssens, Ivan A.
- Nature, Vol. 440, Issue 7081
Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency
journal, October 2011
- Dijkstra, Paul; Thomas, Scott C.; Heinrich, Paul L.
- Soil Biology and Biochemistry, Vol. 43, Issue 10
Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities
journal, October 2007
- Hall, Ek; Cotner, Jb
- Aquatic Microbial Ecology, Vol. 49
A trait-based approach for modelling microbial litter decomposition
journal, May 2012
- Allison, S. D.
- Ecology Letters, Vol. 15, Issue 9
Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures
journal, October 2000
- Devêvre, Olivier C.; Horwáth, William R.
- Soil Biology and Biochemistry, Vol. 32, Issue 11-12
The temperature response of soil microbial efficiency and its feedback to climate
journal, January 2013
- Frey, Serita D.; Lee, Juhwan; Melillo, Jerry M.
- Nature Climate Change, Vol. 3, Issue 4
A Theoretical Model of Litter Decay and Microbial Interaction
journal, May 2006
- Moorhead, Daryl L.; Sinsabaugh, Robert L.
- Ecological Monographs, Vol. 76, Issue 2
Patterns of substrate utilization during long-term incubations at different temperatures
journal, November 2008
- Steinweg, J. Megan; Plante, Alain F.; Conant, Richard T.
- Soil Biology and Biochemistry, Vol. 40, Issue 11
Microbial contributions to climate change through carbon cycle feedbacks
journal, July 2008
- Bardgett, Richard D.; Freeman, Chris; Ostle, Nicholas J.
- The ISME Journal, Vol. 2, Issue 8
Cooperation, Competition, and Coalitions in Enzyme-Producing Microbes: Social Evolution and Nutrient Depolymerization Rates
journal, January 2012
- Folse, Henry J.; Allison, Steven D.
- Frontiers in Microbiology, Vol. 3
Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity
journal, January 2014
- Li, Jianwei; Wang, Gangsheng; Allison, Steven D.
- Biogeochemistry, Vol. 119, Issue 1-3
The effect of temperature on the molar growth yield and maintenance requirement of Escherichia coli W during aerobic growth in continuous culture
journal, September 1976
- Farmer, Ian S.; Jones, Colin W.
- FEBS Letters, Vol. 67, Issue 3
Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain
journal, January 2007
- Trasar-Cepeda, C.; Gil-Sotres, F.; Leirós, M. C.
- Soil Biology and Biochemistry, Vol. 39, Issue 1
Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition
journal, April 2000
- van Ginkel, J. H.; Gorissen, A.; Polci, D.
- Soil Biology and Biochemistry, Vol. 32, Issue 4
Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014
- Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M.
- Biogeosciences, Vol. 11, Issue 14
Climate change alters ecological strategies of soil bacteria
journal, November 2013
- Evans, Sarah E.; Wallenstein, Matthew D.
- Ecology Letters, Vol. 17, Issue 2
The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study
journal, January 2012
- German, Donovan P.; Marcelo, Kathleen R. B.; Stone, Madeleine M.
- Global Change Biology, Vol. 18, Issue 4
The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies
journal, October 2007
- MacLean, R. C.
- Heredity, Vol. 100, Issue 3
Biogenic Carbon Cycling in the Upper Ocean: Effects of Microbial Respiration
journal, March 2001
- Rivkin, R. B.
- Science, Vol. 291, Issue 5512
Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review
journal, July 2012
- Manzoni, Stefano; Taylor, Philip; Richter, Andreas
- New Phytologist, Vol. 196, Issue 1
Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment
journal, September 2009
- Lawrence, Corey R.; Neff, Jason C.; Schimel, Joshua P.
- Soil Biology and Biochemistry, Vol. 41, Issue 9
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model
journal, April 2003
- Schimel, J.
- Soil Biology and Biochemistry, Vol. 35, Issue 4
Bacterial Growth Efficiency in Natural Aquatic Systems
journal, November 1998
- del Giorgio, Paul A.; Cole, Jonathan J.
- Annual Review of Ecology and Systematics, Vol. 29, Issue 1
Emergent Biogeography of Microbial Communities in a Model Ocean
journal, March 2007
- Follows, M. J.; Dutkiewicz, S.; Grant, S.
- Science, Vol. 315, Issue 5820
The trade-off between rate and yield in the design of microbial metabolism
journal, March 2010
- Frank, S. A.
- Journal of Evolutionary Biology, Vol. 23, Issue 3
Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary
journal, July 2006
- Apple, Jk; del Giorgio, Pa; Kemp, Wm
- Aquatic Microbial Ecology, Vol. 43
Comparison of temperature effects on soil respiration and bacterial and fungal growth rates
journal, March 2005
- Pietikåinen, Janna; Pettersson, Marie; Bååth, Erland
- FEMS Microbiology Ecology, Vol. 52, Issue 1
Do growth yield efficiencies differ between soil microbial communities differing in fungal:bacterial ratios? Reality check and methodological issues
journal, April 2006
- Thiet, Rachel K.; Frey, Serita D.; Six, Johan
- Soil Biology and Biochemistry, Vol. 38, Issue 4
Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming?
journal, October 2012
- Tucker, Colin L.; Bell, Jennifer; Pendall, Elise
- Global Change Biology, Vol. 19, Issue 1
Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses
journal, January 2013
- Wang, Gangsheng; Post, Wilfred M.; Mayes, Melanie A.
- Ecological Applications, Vol. 23, Issue 1
Soil-carbon response to warming dependent on microbial physiology
journal, April 2010
- Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A.
- Nature Geoscience, Vol. 3, Issue 5
The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency: Resource quantity/quality drives microbial C-use-efficiency
journal, June 2010
- Keiblinger, Katharina M.; Hall, Edward K.; Wanek, Wolfgang
- FEMS Microbiology Ecology
Thermal adaptation of decomposer communities in warming soils
journal, January 2013
- Bradford, Mark A.
- Frontiers in Microbiology, Vol. 4
Microbial abundance and composition influence litter decomposition response to environmental change
journal, March 2013
- Allison, Steven D.; Lu, Ying; Weihe, Claudia
- Ecology, Vol. 94, Issue 3
Microbial physiology and ecology of slow growth.
journal, January 1997
- Koch, A. L.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 3
Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique
journal, August 2007
- Rousk, Johannes; Bååth, Erland
- Soil Biology and Biochemistry, Vol. 39, Issue 8
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources
journal, January 2014
- Mooshammer, Maria; Wanek, Wolfgang; Zechmeister-Boltenstern, Sophie
- Frontiers in Microbiology, Vol. 5
Temperature responses of enzymes in two forest soils
journal, January 1990
- McClaugherty, C. A.; Linkins, A. E.
- Soil Biology and Biochemistry, Vol. 22, Issue 1
Temperature sensitivity of soil enzyme kinetics under N ‐fertilization in two temperate forests
journal, October 2011
- Stone, Madeleine M.; Weiss, Marissa S.; Goodale, Christine L.
- Global Change Biology, Vol. 18, Issue 3
Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes
journal, October 2006
- Allison, Steven D.
- Biogeochemistry, Vol. 81, Issue 3
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling
journal, April 2013
- Sinsabaugh, Robert L.; Manzoni, Stefano; Moorhead, Daryl L.
- Ecology Letters, Vol. 16, Issue 7
Cooperation and Competition in the Evolution of ATP-Producing Pathways
journal, April 2001
- Pfeiffer, T.; Schuster, S.; Bonhoeffer, S.
- Science, Vol. 292, Issue 5516
A framework for representing microbial decomposition in coupled climate models
journal, August 2011
- Todd-Brown, Katherine E. O.; Hopkins, Francesca M.; Kivlin, Stephanie N.
- Biogeochemistry, Vol. 109, Issue 1-3
Integrating microbial physiology and physiochemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014
- Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M.
- Biogeosciences Discussions, Vol. 11, Issue 1
The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies
journal, October 2007
- MacLean, R. C.
- Heredity, Vol. 100, Issue 5
Feedback interactions between needle litter decomposition and rhizosphere activity
journal, May 2004
- Subke, Jens-Arne; Hahn, Volker; Battipaglia, Giovanna
- Oecologia, Vol. 139, Issue 4
Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes
journal, October 2006
- Allison, Steven D.
- Biogeochemistry, Vol. 81, Issue 3
A framework for representing microbial decomposition in coupled climate models
journal, August 2011
- Todd-Brown, Katherine E. O.; Hopkins, Francesca M.; Kivlin, Stephanie N.
- Biogeochemistry, Vol. 109, Issue 1-3
Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity
journal, January 2014
- Li, Jianwei; Wang, Gangsheng; Allison, Steven D.
- Biogeochemistry, Vol. 119, Issue 1-3
The effect of temperature on the molar growth yield and maintenance requirement of Escherichia coli W during aerobic growth in continuous culture
journal, September 1976
- Farmer, Ian S.; Jones, Colin W.
- FEBS Letters, Vol. 67, Issue 3
Do growth yield efficiencies differ between soil microbial communities differing in fungal:bacterial ratios? Reality check and methodological issues
journal, April 2006
- Thiet, Rachel K.; Frey, Serita D.; Six, Johan
- Soil Biology and Biochemistry, Vol. 38, Issue 4
Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain
journal, January 2007
- Trasar-Cepeda, C.; Gil-Sotres, F.; Leirós, M. C.
- Soil Biology and Biochemistry, Vol. 39, Issue 1
Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique
journal, August 2007
- Rousk, Johannes; Bååth, Erland
- Soil Biology and Biochemistry, Vol. 39, Issue 8
Patterns of substrate utilization during long-term incubations at different temperatures
journal, November 2008
- Steinweg, J. Megan; Plante, Alain F.; Conant, Richard T.
- Soil Biology and Biochemistry, Vol. 40, Issue 11
Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment
journal, September 2009
- Lawrence, Corey R.; Neff, Jason C.; Schimel, Joshua P.
- Soil Biology and Biochemistry, Vol. 41, Issue 9
Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency
journal, October 2011
- Dijkstra, Paul; Thomas, Scott C.; Heinrich, Paul L.
- Soil Biology and Biochemistry, Vol. 43, Issue 10
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
journal, March 2006
- Davidson, Eric A.; Janssens, Ivan A.
- Nature, Vol. 440, Issue 7081
The temperature response of soil microbial efficiency and its feedback to climate
journal, January 2013
- Frey, Serita D.; Lee, Juhwan; Melillo, Jerry M.
- Nature Climate Change, Vol. 3, Issue 4
Soil-carbon response to warming dependent on microbial physiology
journal, April 2010
- Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A.
- Nature Geoscience, Vol. 3, Issue 5
The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies
journal, October 2007
- MacLean, R. C.
- Heredity, Vol. 100, Issue 3
Availability of public goods shapes the evolution of competing metabolic strategies
journal, August 2013
- Bachmann, H.; Fischlechner, M.; Rabbers, I.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 35
The maintenance energy of bacteria in growing cultures
journal, October 1965
- Pirt, S. J.
- Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 163, Issue 991, p. 224-231
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling
journal, April 2013
- Sinsabaugh, Robert L.; Manzoni, Stefano; Moorhead, Daryl L.
- Ecology Letters, Vol. 16, Issue 7
Climate change alters ecological strategies of soil bacteria
journal, November 2013
- Evans, Sarah E.; Wallenstein, Matthew D.
- Ecology Letters, Vol. 17, Issue 2
Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming?
journal, October 2012
- Tucker, Colin L.; Bell, Jennifer; Pendall, Elise
- Global Change Biology, Vol. 19, Issue 1
The trade-off between rate and yield in the design of microbial metabolism
journal, March 2010
- Frank, S. A.
- Journal of Evolutionary Biology, Vol. 23, Issue 3
A trait-based approach for modelling microbial litter decomposition
journal, May 2012
- Allison, S. D.
- Ecology Letters, Vol. 15, Issue 9
Cooperation and Competition in the Evolution of ATP-Producing Pathways
journal, April 2001
- Pfeiffer, T.; Schuster, S.; Bonhoeffer, S.
- Science, Vol. 292, Issue 5516
Emergent Biogeography of Microbial Communities in a Model Ocean
journal, March 2007
- Follows, M. J.; Dutkiewicz, S.; Grant, S.
- Science, Vol. 315, Issue 5820
Biogenic Carbon Cycling in the Upper Ocean: Effects of Microbial Respiration
journal, March 2001
- Rivkin, R. B.
- Science, Vol. 291, Issue 5512
Effects of growth temperature on yield and maintenance during glucose-limited continuous culture of Escherichia coli.
journal, January 1976
- Mainzer, S. E.; Hempfling, W. P.
- Journal of Bacteriology, Vol. 126, Issue 1
Microbial Physiology and Ecology of Slow Growth
journal, March 1998
- Koch, Arthur L.
- Microbiology and Molecular Biology Reviews, Vol. 62, Issue 1
Bacterial Growth Efficiency in Natural Aquatic Systems
journal, November 1998
- del Giorgio, Paul A.; Cole, Jonathan J.
- Annual Review of Ecology and Systematics, Vol. 29, Issue 1
Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses
journal, January 2013
- Wang, Gangsheng; Post, Wilfred M.; Mayes, Melanie A.
- Ecological Applications, Vol. 23, Issue 1
Microbial abundance and composition influence litter decomposition response to environmental change
journal, March 2013
- Allison, Steven D.; Lu, Ying; Weihe, Claudia
- Ecology, Vol. 94, Issue 3
Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities
journal, October 2007
- Hall, Ek; Cotner, Jb
- Aquatic Microbial Ecology, Vol. 49
Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary
journal, July 2006
- Apple, Jk; del Giorgio, Pa; Kemp, Wm
- Aquatic Microbial Ecology, Vol. 43
Cooperation, Competition, and Coalitions in Enzyme-Producing Microbes: Social Evolution and Nutrient Depolymerization Rates
journal, January 2012
- Folse, Henry J.; Allison, Steven D.
- Frontiers in Microbiology, Vol. 3
Thermal adaptation of decomposer communities in warming soils
journal, January 2013
- Bradford, Mark A.
- Frontiers in Microbiology, Vol. 4
Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources
journal, January 2014
- Mooshammer, Maria; Wanek, Wolfgang; Zechmeister-Boltenstern, Sophie
- Frontiers in Microbiology, Vol. 5
Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014
- Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M.
- Biogeosciences, Vol. 11, Issue 14
Works referencing / citing this record:
Role of carbon allocation efficiency in the temperature dependence of autotroph growth rates
journal, July 2018
- García-Carreras, Bernardo; Sal, Sofía; Padfield, Daniel
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 31
Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton
journal, November 2015
- Padfield, Daniel; Yvon-Durocher, Genevieve; Buckling, Angus
- Ecology Letters, Vol. 19, Issue 2
Rate of warming affects temperature sensitivity of anaerobic peat decomposition and greenhouse gas production
journal, September 2017
- Sihi, Debjani; Inglett, Patrick W.; Gerber, Stefan
- Global Change Biology, Vol. 24, Issue 1
Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming
journal, May 2018
- Alvarez, Gaël; Shahzad, Tanvir; Andanson, Laurence
- Global Change Biology, Vol. 24, Issue 9
Reduced carbon use efficiency and increased microbial turnover with soil warming
journal, December 2018
- Li, Jianwei; Wang, Gangsheng; Mayes, Melanie A.
- Global Change Biology
Comparing models of microbial–substrate interactions and their response to warming
journal, January 2016
- Sihi, Debjani; Gerber, Stefan; Inglett, Patrick W.
- Biogeosciences, Vol. 13, Issue 6
Reviews and syntheses: Carbon use efficiency from organisms to ecosystems – definitions, theories, and empirical evidence
journal, January 2018
- Manzoni, Stefano; Čapek, Petr; Porada, Philipp
- Biogeosciences, Vol. 15, Issue 19
Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world
journal, January 2019
- Pold, Grace; Sistla, Seeta A.; DeAngelis, Kristen M.
- Biogeosciences, Vol. 16, Issue 24
The complex relationship between microbial growth rate and yield and its implications for ecosystem processes
journal, June 2015
- Lipson, David A.
- Frontiers in Microbiology, Vol. 6
Enzymatic Strategies and Carbon Use Efficiency of a Litter-Decomposing Fungus Grown on Maize Leaves, Stems, and Roots
journal, August 2016
- Lashermes, Gwenaëlle; Gainvors-Claisse, Angélique; Recous, Sylvie
- Frontiers in Microbiology, Vol. 7
Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward
journal, May 2019
- Kallenbach, Cynthia M.; Wallenstein, Matthew D.; Schipanksi, Meagan E.
- Frontiers in Microbiology, Vol. 10