Reduced carbon use efficiency and increased microbial turnover with soil warming
Abstract
Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial-enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades-long field observations, contrast with values obtained from short-term laboratory experiments. We also show that long-term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion-derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of <1.0% on average (1st and 3rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadalmore »
- Authors:
-
[1];
[2];
[4];
- Tennessee State Univ., Nashville, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Oklahoma, Norman, OK (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of California, Irvine, CA (United States)
- Univ. of New Hampshire, Durham, NH (United States)
- Univ. of Oklahoma, Norman, OK (United States)
- Northern Arizona Univ., Flagstaff, AZ (United States)
- Marine Biological Lab., Woods Hole, MA (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1505337
- Alternate Identifier(s):
- OSTI ID: 1485699
- Grant/Contract Number:
- AC05-00OR22725; SC0014374; FC02-06ER64157; SC0010740; SC0016590
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Volume: 25; Journal Issue: 3; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; carbon use efficiency (CUE); data‐model integration; Harvard forest; microbial biomass turnover (rB); soil warming; temperature sensitivity
Citation Formats
Li, Jianwei, Wang, Gangsheng, Mayes, Melanie A., Allison, Steven D., Frey, Serita D., Shi, Zheng, Hu, Xiao ‐Ming, Luo, Yiqi, and Melillo, Jerry M. Reduced carbon use efficiency and increased microbial turnover with soil warming. United States: N. p., 2018.
Web. doi:10.1111/gcb.14517.
Li, Jianwei, Wang, Gangsheng, Mayes, Melanie A., Allison, Steven D., Frey, Serita D., Shi, Zheng, Hu, Xiao ‐Ming, Luo, Yiqi, & Melillo, Jerry M. Reduced carbon use efficiency and increased microbial turnover with soil warming. United States. https://doi.org/10.1111/gcb.14517
Li, Jianwei, Wang, Gangsheng, Mayes, Melanie A., Allison, Steven D., Frey, Serita D., Shi, Zheng, Hu, Xiao ‐Ming, Luo, Yiqi, and Melillo, Jerry M. Mon .
"Reduced carbon use efficiency and increased microbial turnover with soil warming". United States. https://doi.org/10.1111/gcb.14517. https://www.osti.gov/servlets/purl/1505337.
@article{osti_1505337,
title = {Reduced carbon use efficiency and increased microbial turnover with soil warming},
author = {Li, Jianwei and Wang, Gangsheng and Mayes, Melanie A. and Allison, Steven D. and Frey, Serita D. and Shi, Zheng and Hu, Xiao ‐Ming and Luo, Yiqi and Melillo, Jerry M.},
abstractNote = {Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial-enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades-long field observations, contrast with values obtained from short-term laboratory experiments. We also show that long-term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion-derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of <1.0% on average (1st and 3rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadal datasets. This approach can potentially be applied in broader spatiotemporal scales to improve long-term projections of soil C feedbacks to climate warming.},
doi = {10.1111/gcb.14517},
journal = {Global Change Biology},
number = 3,
volume = 25,
place = {United States},
year = {Mon Nov 12 00:00:00 EST 2018},
month = {Mon Nov 12 00:00:00 EST 2018}
}
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Works referenced in this record:
Deconvolution analysis to quantify autotrophic and heterotrophic respiration and their temperature sensitivities
journal, August 2010
- Luo, Yiqi; Zhou, Xuhui
- New Phytologist, Vol. 188, Issue 1
Soil warming and trace gas fluxes: experimental design and preliminary flux results
journal, February 1993
- Peterjohn, William T.; Melillo, Jerry M.; Bowles, Francis P.
- Oecologia, Vol. 93, Issue 1
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
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 mediation of carbon-cycle feedbacks to climate warming
journal, December 2011
- Zhou, Jizhong; Xue, Kai; Xie, Jianping
- Nature Climate Change, Vol. 2, Issue 2
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
Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils
journal, April 2011
- Brzostek, Edward R.; Finzi, Adrien C.
- Ecology, Vol. 92, Issue 4
Environmental stress response limits microbial necromass contributions to soil organic carbon
journal, June 2015
- Crowther, Thomas W.; Sokol, Noah W.; Oldfield, Emily E.
- Soil Biology and Biochemistry, Vol. 85
Elucidation of the source and turnover of water soluble and microbial biomass carbon in agricultural soils
journal, May 2000
- Gregorich, E. G.; Liang, B. C.; Drury, C. F.
- Soil Biology and Biochemistry, Vol. 32, Issue 5
Microbial physiology and soil CO 2 efflux after 9 years of soil warming in a temperate forest - no indications for thermal adaptations
journal, September 2015
- Schindlbacher, Andreas; Schnecker, Jörg; Takriti, Mounir
- Global Change Biology, Vol. 21, Issue 11
Nitrogen fertilization decreases forest soil fungal and bacterial biomass in three long-term experiments
journal, February 2006
- Wallenstein, Matthew D.; McNulty, Steven; Fernandez, Ivan J.
- Forest Ecology and Management, Vol. 222, Issue 1-3
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
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
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
Turnover of carbon through the microbial biomass in soils with different texture
journal, January 1991
- Gregorich, E. G.; Voroney, R. P.; Kachanoski, R. G.
- Soil Biology and Biochemistry, Vol. 23, Issue 8
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
Separating cellular metabolism from exoenzyme activity in soil organic matter decomposition
journal, April 2014
- Blankinship, Joseph C.; Becerra, Caryl A.; Schaeffer, Sean M.
- Soil Biology and Biochemistry, Vol. 71
Soil respiration does not acclimatize to warmer temperatures when modeled over seasonal timescales
journal, June 2012
- Contosta, A. R.; Frey, S. D.; Ollinger, S. V.
- Biogeochemistry, Vol. 112, Issue 1-3
Statistical analysis in the estimation of maintenance and true growth yield coefficients
journal, April 1984
- Fieschko, John; Humphrey, Arthur E.
- Biotechnology and Bioengineering, Vol. 26, Issue 4
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
Ecological forecasting and data assimilation in a data-rich era
journal, July 2011
- Luo, Yiqi; Ogle, Kiona; Tucker, Colin
- Ecological Applications, Vol. 21, Issue 5
The role of data assimilation in predictive ecology
journal, May 2014
- Niu, Shuli; Luo, Yiqi; Dietze, Michael C.
- Ecosphere, Vol. 5, Issue 5
Optimal metabolic regulation along resource stoichiometry gradients
journal, July 2017
- Manzoni, Stefano; Čapek, Petr; Mooshammer, Maria
- Ecology Letters, Vol. 20, Issue 9
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world
journal, October 2017
- Melillo, J. M.; Frey, S. D.; DeAngelis, K. M.
- Science, Vol. 358, Issue 6359
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
Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter
journal, February 2016
- Geyer, Kevin M.; Kyker-Snowman, Emily; Grandy, A. Stuart
- Biogeochemistry, Vol. 127, Issue 2-3
Differential effects of warming and nitrogen fertilization on soil respiration and microbial dynamics in switchgrass croplands
journal, April 2018
- Li, Jianwei; Jian, Siyang; de Koff, Jason P.
- GCB Bioenergy, Vol. 10, Issue 8
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
Microbial models with data-driven parameters predict stronger soil carbon responses to climate change
journal, March 2015
- Hararuk, Oleksandra; Smith, Matthew J.; Luo, Yiqi
- Global Change Biology, Vol. 21, Issue 6
Microbial community response to varying magnitudes of desiccation in soil: A test of the osmolyte accumulation hypothesis
journal, February 2013
- Kakumanu, Madhavi L.; Cantrell, Charles L.; Williams, Mark A.
- Soil Biology and Biochemistry, Vol. 57
Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils
journal, March 2011
- Contosta, A. R.; Frey, S. D.; Cooper, A. B.
- Ecosphere, Vol. 2, Issue 3
Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest
journal, July 1993
- Bowden, Richard D.; Nadelhoffer, Knute J.; Boone, Richard D.
- Canadian Journal of Forest Research, Vol. 23, Issue 7
Soil microbial carbon turnover decreases with increasing molecular size
journal, July 2013
- Malik, Ashish; Blagodatskaya, Evgenia; Gleixner, Gerd
- Soil Biology and Biochemistry, Vol. 62
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
Long-term sensitivity of soil carbon turnover to warming
journal, January 2005
- Knorr, W.; Prentice, I. C.; House, J. I.
- Nature, Vol. 433, Issue 7023
A Bayesian approach to stochastic capture zone delineation incorporating tracer arrival times, conductivity measurements, and hydraulic head observations: A BAYESIAN APPROACH TO CAPTURE ZONE DELINEATION
journal, May 2003
- Feyen, L.; Gómez-Hernández, J. J.; Ribeiro, P. J.
- Water Resources Research, Vol. 39, Issue 5
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
Global pattern and controls of soil microbial metabolic quotient
journal, May 2017
- Xu, Xiaofeng; Schimel, Joshua P.; Janssens, Ivan A.
- Ecological Monographs, Vol. 87, Issue 3
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
Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest
journal, July 2004
- Compton, Jana E.; Watrud, Lidia S.; Arlene Porteous, L.
- Forest Ecology and Management, Vol. 196, Issue 1
A theoretical reassessment of microbial maintenance and implications for microbial ecology modeling
journal, April 2012
- Wang, Gangsheng; Post, Wilfred M.
- FEMS Microbiology Ecology, Vol. 81, Issue 3
Why environmental scientists are becoming Bayesians: Modelling with Bayes
journal, December 2004
- Clark, James S.
- Ecology Letters, Vol. 8, Issue 1
Accelerated microbial turnover but constant growth efficiency with warming in soil
journal, September 2014
- Hagerty, Shannon B.; van Groenigen, Kees Jan; Allison, Steven D.
- Nature Climate Change, Vol. 4, Issue 10
The contentious nature of soil organic matter
journal, November 2015
- Lehmann, Johannes; Kleber, Markus
- Nature, Vol. 528, Issue 7580
Modeling adaptation of carbon use efficiency in microbial communities
journal, October 2014
- Allison, Steven D.
- Frontiers in Microbiology, Vol. 5
Changes in soil microbial biomass, metabolic quotient, and organic matter turnover under Hieracium ( H. pilosella L.)
journal, December 1999
- Saggar, S.; McIntosh, P. D.; Hedley, C. B.
- Biology and Fertility of Soils, Vol. 30, Issue 3
Toward more realistic projections of soil carbon dynamics by Earth system models: SOIL CARBON MODELING
journal, January 2016
- Luo, Yiqi; Ahlström, Anders; Allison, Steven D.
- Global Biogeochemical Cycles, Vol. 30, Issue 1
Parameter estimation for models of ligninolytic and cellulolytic enzyme kinetics
journal, May 2012
- Wang, Gangsheng; Post, Wilfred M.; Mayes, Melanie A.
- Soil Biology and Biochemistry, Vol. 48
Thermal acclimation in widespread heterotrophic soil microbes
journal, January 2013
- Crowther, Thomas W.; Bradford, Mark A.
- Ecology Letters, Vol. 16, Issue 4
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
Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002
- Melillo, J. M.
- Science, Vol. 298, Issue 5601
Microbial seed banks: the ecological and evolutionary implications of dormancy
journal, January 2011
- Lennon, Jay T.; Jones, Stuart E.
- Nature Reviews Microbiology, Vol. 9, Issue 2
Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils
journal, January 2002
- Six, J.; Conant, R. T.; Paul, E. A.
- Plant and Soil, Vol. 241, Issue 2, p. 155-176
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
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
Temperature acclimation and adaptation of enzyme physiology in Neurospora discreta
journal, October 2018
- Allison, Steven D.; Romero-Olivares, Adriana L.; Lu, Lucy
- Fungal Ecology, Vol. 35
Thermal adaptation of decomposer communities in warming soils
journal, January 2013
- Bradford, Mark A.
- Frontiers in Microbiology, Vol. 4
Probabilistic inversion of a terrestrial ecosystem model: Analysis of uncertainty in parameter estimation and model prediction: PROBABILISTIC INVERSION OF TERRESTRIAL ECOSYSTEM
journal, May 2006
- Xu, Tao; White, Luther; Hui, Dafeng
- Global Biogeochemical Cycles, Vol. 20, Issue 2
Thermal adaptation of soil microbial respiration to elevated temperature
journal, December 2008
- Bradford, Mark A.; Davies, Christian A.; Frey, Serita D.
- Ecology Letters, Vol. 11, Issue 12
Survival of the soil microbial biomass at elevated temperatures
journal, January 1990
- Joergensen, R. G.; Brookes, P. C.; Jenkinson, D. S.
- Soil Biology and Biochemistry, Vol. 22, Issue 8
Microbial biomass, functional capacity, and community structure after 12 years of soil warming
journal, November 2008
- Frey, S. D.; Drijber, R.; Smith, H.
- Soil Biology and Biochemistry, Vol. 40, Issue 11
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
Application macroscopic principles to microbial metabolism
journal, May 2009
- Roels, J. A.; Jens Nielsen, Introduction by
- Biotechnology and Bioengineering, Vol. 103, Issue 1
Works referencing / citing this record:
Priming of soil organic carbon decomposition induced by exogenous organic carbon input: a meta-analysis
journal, August 2019
- Sun, Zhaolin; Liu, Shengen; Zhang, Tianan
- Plant and Soil, Vol. 443, Issue 1-2
Soil microbial biomass increases along elevational gradients in the tropics and subtropics but not elsewhere
journal, October 2019
- He, Xianjin; Hou, Enqing; Veen, G. F.
- Global Ecology and Biogeography, Vol. 29, Issue 2
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