Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world
Abstract
Abstract. Climate change has the potential to destabilize the Earth's massive terrestrial carbon (C) stocks, but the degree to which models project this destabilization to occur depends on the kinds and complexities of microbial processes they simulate. Of particular note is carbon use efficiency (CUE), which determines the fraction of C processed by microbes that is anabolized into microbial biomass rather than lost to the atmosphere and soil as carbon dioxide and extracellular products. The temperature sensitivity of CUE is often modeled as an intrinsically fixed (homogeneous) property of the community, which contrasts with empirical data and has unknown impacts on projected changes to the soil C cycle under global warming. We used the Decomposition Model of Enzymatic Traits (DEMENT) – which simulates taxon-level litter decomposition dynamics – to explore the effects of introducing organism-level heterogeneity into the CUE response to temperature for decomposition of leaf litter under 5 ∘C of warming. We found that allowing the CUE temperature response to differ between taxa facilitated increased loss of litter C, unless fungal taxa were specifically restricted to decreasing CUE with temperature. Litter C loss was exacerbated by variable and elevated CUE at higher temperature, which effectively lowered costs for extracellular enzymemore »
- Publication Date:
- Research Org.:
- Univ. of Massachusetts, Amherst, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1580139
- Alternate Identifier(s):
- OSTI ID: 1803061
- Grant/Contract Number:
- SC0016590
- Resource Type:
- Published Article
- Journal Name:
- Biogeosciences (Online)
- Additional Journal Information:
- Journal Name: Biogeosciences (Online) Journal Volume: 16 Journal Issue: 24; Journal ID: ISSN 1726-4189
- Publisher:
- Copernicus Publications, EGU
- Country of Publication:
- Germany
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 58 GEOSCIENCES; Environmental Sciences & Ecology; Geology
Citation Formats
Pold, Grace, Sistla, Seeta A., and DeAngelis, Kristen M. Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world. Germany: N. p., 2019.
Web. doi:10.5194/bg-16-4875-2019.
Pold, Grace, Sistla, Seeta A., & DeAngelis, Kristen M. Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world. Germany. https://doi.org/10.5194/bg-16-4875-2019
Pold, Grace, Sistla, Seeta A., and DeAngelis, Kristen M. Fri .
"Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world". Germany. https://doi.org/10.5194/bg-16-4875-2019.
@article{osti_1580139,
title = {Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world},
author = {Pold, Grace and Sistla, Seeta A. and DeAngelis, Kristen M.},
abstractNote = {Abstract. Climate change has the potential to destabilize the Earth's massive terrestrial carbon (C) stocks, but the degree to which models project this destabilization to occur depends on the kinds and complexities of microbial processes they simulate. Of particular note is carbon use efficiency (CUE), which determines the fraction of C processed by microbes that is anabolized into microbial biomass rather than lost to the atmosphere and soil as carbon dioxide and extracellular products. The temperature sensitivity of CUE is often modeled as an intrinsically fixed (homogeneous) property of the community, which contrasts with empirical data and has unknown impacts on projected changes to the soil C cycle under global warming. We used the Decomposition Model of Enzymatic Traits (DEMENT) – which simulates taxon-level litter decomposition dynamics – to explore the effects of introducing organism-level heterogeneity into the CUE response to temperature for decomposition of leaf litter under 5 ∘C of warming. We found that allowing the CUE temperature response to differ between taxa facilitated increased loss of litter C, unless fungal taxa were specifically restricted to decreasing CUE with temperature. Litter C loss was exacerbated by variable and elevated CUE at higher temperature, which effectively lowered costs for extracellular enzyme production. Together these results implicate a role for diversity of taxon-level CUE responses in driving the fate of litter C in a warmer world within DEMENT, which should be explored within the framework of additional model structures and validated with empirical studies.},
doi = {10.5194/bg-16-4875-2019},
journal = {Biogeosciences (Online)},
number = 24,
volume = 16,
place = {Germany},
year = {2019},
month = {12}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.5194/bg-16-4875-2019
https://doi.org/10.5194/bg-16-4875-2019
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
A meta-analysis of temperature sensitivity as a microbial trait
journal, July 2018
- Alster, Charlotte J.; Weller, Zachary D.; von Fischer, Joseph C.
- Global Change Biology, Vol. 24, Issue 9
Consequences of drought tolerance traits for microbial decomposition in the DEMENT model
journal, April 2017
- Allison, Steven D.; Goulden, Michael L.
- Soil Biology and Biochemistry, Vol. 107
Microbial temperature sensitivity and biomass change explain soil carbon loss with warming
journal, September 2018
- Walker, Tom W. N.; Kaiser, Christina; Strasser, Florian
- Nature Climate Change, Vol. 8, Issue 10
Leaf Litter Mixtures Alter Microbial Community Development: Mechanisms for Non-Additive Effects in Litter Decomposition
journal, April 2013
- Chapman, Samantha K.; Newman, Gregory S.; Hart, Stephen C.
- PLoS ONE, Vol. 8, Issue 4
Direct Evidence for Temporal Molecular Fractionation of Dissolved Organic Matter at the Iron Oxyhydroxide Interface
journal, December 2018
- Coward, Elizabeth K.; Ohno, Tsutomu; Sparks, Donald L.
- Environmental Science & Technology, Vol. 53, Issue 2
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
Evaluating soil microbial carbon use efficiency explicitly as a function of cellular processes: implications for measurements and models
journal, August 2018
- Hagerty, Shannon B.; Allison, Steven D.; Schimel, Joshua P.
- Biogeochemistry, Vol. 140, Issue 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
Clarifying the interpretation of carbon use efficiency in soil through methods comparison
journal, January 2019
- Geyer, Kevin M.; Dijkstra, Paul; Sinsabaugh, Robert
- Soil Biology and Biochemistry, Vol. 128
Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems
journal, January 2006
- Six, J.; Frey, S. D.; Thiet, R. K.
- Soil Science Society of America Journal, Vol. 70, Issue 2
Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
journal, January 2020
- Pold, Grace; Domeignoz-Horta, Luiz A.; Morrison, Eric W.
- mBio, Vol. 11, Issue 1
Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland
journal, June 2016
- Spohn, Marie; Pötsch, Erich M.; Eichorst, Stephanie A.
- Soil Biology and Biochemistry, Vol. 97
Bacterial growth efficiency varies in soils under different land management practices
journal, February 2014
- Lee, Zarraz M.; Schmidt, Thomas M.
- Soil Biology and Biochemistry, Vol. 69
Decoupling the direct and indirect effects of climate on plant litter decomposition: Accounting for stress-induced modifications in plant chemistry
journal, January 2018
- Suseela, Vidya; Tharayil, Nishanth
- Global Change Biology, Vol. 24, Issue 4
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
Substrate identity and amount overwhelm temperature effects on soil carbon formation
journal, September 2018
- Oldfield, Emily E.; Crowther, Thomas W.; Bradford, Mark A.
- Soil Biology and Biochemistry, Vol. 124
Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally
journal, July 2019
- Ye, Jian‐Sheng; Bradford, Mark A.; Dacal, Marina
- Global Change Biology, Vol. 25, Issue 10
Stoichiometry of microbial carbon use efficiency in soils
journal, May 2016
- Sinsabaugh, Robert L.; Turner, Benjamin L.; Talbot, Jennifer M.
- Ecological Monographs, Vol. 86, Issue 2
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
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls
journal, November 2016
- Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart
- Nature Communications, Vol. 7, Issue 1
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
Land use driven change in soil pH affects microbial carbon cycling processes
journal, September 2018
- Malik, Ashish A.; Puissant, Jeremy; Buckeridge, Kate M.
- Nature Communications, Vol. 9, Issue 1
Modeling soil metabolic processes using isotopologue pairs of position-specific 13C-labeled glucose and pyruvate
journal, September 2011
- Dijkstra, Paul; Dalder, Jacob J.; Selmants, Paul C.
- Soil Biology and Biochemistry, Vol. 43, Issue 9
Fitting Linear Mixed-Effects Models Using lme4
journal, January 2015
- Bates, Douglas; Mächler, Martin; Bolker, Ben
- Journal of Statistical Software, Vol. 67, Issue 1
Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production
journal, February 2017
- Sinsabaugh, Robert L.; Moorhead, Daryl L.; Xu, Xiaofeng
- New Phytologist, Vol. 214, Issue 4
Temperature sensitivities of extracellular enzyme V max and K m across thermal environments
journal, February 2018
- Allison, Steven D.; Romero-Olivares, Adriana L.; Lu, Ying
- Global Change Biology, Vol. 24, Issue 7
A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems: Global soil microbial biomass C, N and P
journal, December 2012
- Xu, Xiaofeng; Thornton, Peter E.; Post, Wilfred M.
- Global Ecology and Biogeography, Vol. 22, Issue 6
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
A trait-based approach for modelling microbial litter decomposition
journal, May 2012
- Allison, S. D.
- Ecology Letters, Vol. 15, Issue 9
Soil microbial communities with greater investment in resource acquisition have lower growth yield
journal, May 2019
- Malik, Ashish A.; Puissant, Jeremy; Goodall, Tim
- Soil Biology and Biochemistry, Vol. 132
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
Representing life in the Earth system with soil microbial functional traits in the MIMICS model
journal, January 2015
- Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M.
- Geoscientific Model Development, Vol. 8, Issue 6
The effect of temperature and substrate quality on the carbon use efficiency of saprotrophic decomposition
journal, November 2016
- Öquist, Mats G.; Erhagen, Björn; Haei, Mahsa
- Plant and Soil, Vol. 414, Issue 1-2
Modeling adaptation of carbon use efficiency in microbial communities
journal, October 2014
- Allison, Steven D.
- Frontiers in Microbiology, Vol. 5
Global negative vegetation feedback to climate warming responses of leaf litter decomposition rates in cold biomes
journal, July 2007
- Cornelissen, Johannes H. C.; van Bodegom, Peter M.; Aerts, Rien
- Ecology Letters, Vol. 10, Issue 7
The Cost of Protein Production
journal, January 2016
- Kafri, Moshe; Metzl-Raz, Eyal; Jona, Ghil
- Cell Reports, Vol. 14, Issue 1
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
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
Soil Fungal:Bacterial Ratios Are Linked to Altered Carbon Cycling
journal, August 2016
- Malik, Ashish A.; Chowdhury, Somak; Schlager, Veronika
- Frontiers in Microbiology, Vol. 7
Microbial carbon use efficiency and biomass turnover times depending on soil depth – Implications for carbon cycling
journal, May 2016
- Spohn, Marie; Klaus, Karoline; Wanek, Wolfgang
- Soil Biology and Biochemistry, Vol. 96
Reduced carbon use efficiency and increased microbial turnover with soil warming
journal, December 2018
- Li, Jianwei; Wang, Gangsheng; Mayes, Melanie A.
- Global Change Biology
Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015
- DeAngelis, Kristen M.; Pold, Grace; Topçuoğlu, Begüm D.
- Frontiers in Microbiology, Vol. 6
Responses of a tundra system to warming using SCAMPS: a stoichiometrically coupled, acclimating microbe–plant–soil model
journal, February 2014
- Sistla, Seeta A.; Rastetter, Edward B.; Schimel, Joshua P.
- Ecological Monographs, Vol. 84, Issue 1
Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions
journal, November 2014
- Tang, Jinyun; Riley, William J.
- Nature Climate Change, Vol. 5, Issue 1
Soil Microbial Communities Beneath Populus Grandidentata Grown Under Elevated Atmospheric CO 2
journal, February 1996
- Zak, Donald R.; Ringelberg, David B.; Pregitzer, Kurt S.
- Ecological Applications, Vol. 6, Issue 1
Microbial control over carbon cycling in soil
journal, January 2012
- Schimel, Joshua P.; Schaeffer, Sean M.
- Frontiers in Microbiology, Vol. 3
Metabolic costs of amino acid and protein production in Escherichia coli
journal, July 2013
- Kaleta, Christoph; Schäuble, Sascha; Rinas, Ursula
- Biotechnology Journal, Vol. 8, Issue 9
Explicitly representing soil microbial processes in Earth system models: Soil microbes in earth system models
journal, October 2015
- Wieder, William R.; Allison, Steven D.; Davidson, Eric A.
- Global Biogeochemical Cycles, Vol. 29, Issue 10
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
Changes in substrate availability drive carbon cycle response to chronic warming
journal, July 2017
- Pold, Grace; Grandy, A. Stuart; Melillo, Jerry M.
- Soil Biology and Biochemistry, Vol. 110
Soil microbial biomass and organic matter fractions during transition from conventional to organic farming systems
journal, January 2012
- Santos, Valdinar B.; Araújo, Ademir S. F.; Leite, Luiz F. C.
- Geoderma, Vol. 170
Microbial Growth and Carbon Use Efficiency in the Rhizosphere and Root-Free Soil
journal, April 2014
- Blagodatskaya, Evgenia; Blagodatsky, Sergey; Anderson, Traute-Heidi
- PLoS ONE, Vol. 9, Issue 4
Soil warming, carbon-nitrogen interactions, and forest carbon budgets
journal, May 2011
- Melillo, J. M.; Butler, S.; Johnson, J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 23
On the concept of a psychrophile
journal, September 2015
- Cavicchioli, Ricardo
- The ISME Journal, Vol. 10, Issue 4
Extracellular enzyme production and cheating in Pseudomonas fluorescens depend on diffusion rates
journal, April 2014
- Allison, Steven D.; Lu, Lucy; Kent, Alyssa G.
- Frontiers in Microbiology, Vol. 5
Effects of dispersal and selection on stochastic assembly in microbial communities
journal, August 2016
- Evans, Sarah; Martiny, Jennifer B. H.; Allison, Steven D.
- The ISME Journal, Vol. 11, Issue 1
Responses of ecosystem carbon cycle to experimental warming: a meta-analysis
journal, March 2013
- Lu, Meng; Zhou, Xuhui; Yang, Qiang
- Ecology, Vol. 94, Issue 3
Vegetation exerts a greater control on litter decomposition than climate warming in peatlands
journal, January 2015
- Ward, Susan E.; Orwin, Kate H.; Ostle, Nicholas J.
- Ecology, Vol. 96, Issue 1
Global variation of soil microbial carbon-use efficiency in relation to growth temperature and substrate supply
journal, April 2019
- Qiao, Yang; Wang, Jing; Liang, Guopeng
- Scientific Reports, Vol. 9, Issue 1
Growth explains microbial carbon use efficiency across soils differing in land use and geology
journal, January 2019
- Zheng, Qing; Hu, Yuntao; Zhang, Shasha
- Soil Biology and Biochemistry, Vol. 128