Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming
Abstract
Abstract Soil microbial respiration is an important source of uncertainty in projecting future climate and carbon (C) cycle feedbacks. However, its feedbacks to climate warming and underlying microbial mechanisms are still poorly understood. Here we show that the temperature sensitivity of soil microbial respiration ( Q 10 ) in a temperate grassland ecosystem persistently decreases by 12.0 ± 3.7% across 7 years of warming. Also, the shifts of microbial communities play critical roles in regulating thermal adaptation of soil respiration. Incorporating microbial functional gene abundance data into a microbially-enabled ecosystem model significantly improves the modeling performance of soil microbial respiration by 5–19%, and reduces model parametric uncertainty by 55–71%. In addition, modeling analyses show that the microbial thermal adaptation can lead to considerably less heterotrophic respiration (11.6 ± 7.5%), and hence less soil C loss. If such microbially mediated dampening effects occur generally across different spatial and temporal scales, the potential positive feedback of soil microbial respiration in response to climate warming may be less than previously predicted.
- Authors:
-
;
;
;
;
;
;
;
more »
- Publication Date:
- Research Org.:
- Univ. of Oklahoma, Norman, OK (United States)
- Sponsoring Org.:
- USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
- OSTI Identifier:
- 1668434
- Alternate Identifier(s):
- OSTI ID: 1801595
- Grant/Contract Number:
- SC0004601; SC0010715
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Science & Technology - Other Topics
Citation Formats
Guo, Xue, Gao, Qun, Yuan, Mengting, Wang, Gangsheng, Zhou, Xishu, Feng, Jiajie, Shi, Zhou, Hale, Lauren, Wu, Linwei, Zhou, Aifen, Tian, Renmao, Liu, Feifei, Wu, Bo, Chen, Lijun, Jung, Chang Gyo, Niu, Shuli, Li, Dejun, Xu, Xia, Jiang, Lifen, Escalas, Arthur, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Ning, Daliang, Liu, Xueduan, Yang, Yunfeng, Schuur, Edward. A. G., Konstantinidis, Konstantinos T., Cole, James R., Penton, C. Ryan, Luo, Yiqi, Tiedje, James M., and Zhou, Jizhong. Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-18706-z.
Guo, Xue, Gao, Qun, Yuan, Mengting, Wang, Gangsheng, Zhou, Xishu, Feng, Jiajie, Shi, Zhou, Hale, Lauren, Wu, Linwei, Zhou, Aifen, Tian, Renmao, Liu, Feifei, Wu, Bo, Chen, Lijun, Jung, Chang Gyo, Niu, Shuli, Li, Dejun, Xu, Xia, Jiang, Lifen, Escalas, Arthur, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Ning, Daliang, Liu, Xueduan, Yang, Yunfeng, Schuur, Edward. A. G., Konstantinidis, Konstantinos T., Cole, James R., Penton, C. Ryan, Luo, Yiqi, Tiedje, James M., & Zhou, Jizhong. Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming. United Kingdom. https://doi.org/10.1038/s41467-020-18706-z
Guo, Xue, Gao, Qun, Yuan, Mengting, Wang, Gangsheng, Zhou, Xishu, Feng, Jiajie, Shi, Zhou, Hale, Lauren, Wu, Linwei, Zhou, Aifen, Tian, Renmao, Liu, Feifei, Wu, Bo, Chen, Lijun, Jung, Chang Gyo, Niu, Shuli, Li, Dejun, Xu, Xia, Jiang, Lifen, Escalas, Arthur, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Ning, Daliang, Liu, Xueduan, Yang, Yunfeng, Schuur, Edward. A. G., Konstantinidis, Konstantinos T., Cole, James R., Penton, C. Ryan, Luo, Yiqi, Tiedje, James M., and Zhou, Jizhong. Tue .
"Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming". United Kingdom. https://doi.org/10.1038/s41467-020-18706-z.
@article{osti_1668434,
title = {Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming},
author = {Guo, Xue and Gao, Qun and Yuan, Mengting and Wang, Gangsheng and Zhou, Xishu and Feng, Jiajie and Shi, Zhou and Hale, Lauren and Wu, Linwei and Zhou, Aifen and Tian, Renmao and Liu, Feifei and Wu, Bo and Chen, Lijun and Jung, Chang Gyo and Niu, Shuli and Li, Dejun and Xu, Xia and Jiang, Lifen and Escalas, Arthur and Wu, Liyou and He, Zhili and Van Nostrand, Joy D. and Ning, Daliang and Liu, Xueduan and Yang, Yunfeng and Schuur, Edward. A. G. and Konstantinidis, Konstantinos T. and Cole, James R. and Penton, C. Ryan and Luo, Yiqi and Tiedje, James M. and Zhou, Jizhong},
abstractNote = {Abstract Soil microbial respiration is an important source of uncertainty in projecting future climate and carbon (C) cycle feedbacks. However, its feedbacks to climate warming and underlying microbial mechanisms are still poorly understood. Here we show that the temperature sensitivity of soil microbial respiration ( Q 10 ) in a temperate grassland ecosystem persistently decreases by 12.0 ± 3.7% across 7 years of warming. Also, the shifts of microbial communities play critical roles in regulating thermal adaptation of soil respiration. Incorporating microbial functional gene abundance data into a microbially-enabled ecosystem model significantly improves the modeling performance of soil microbial respiration by 5–19%, and reduces model parametric uncertainty by 55–71%. In addition, modeling analyses show that the microbial thermal adaptation can lead to considerably less heterotrophic respiration (11.6 ± 7.5%), and hence less soil C loss. If such microbially mediated dampening effects occur generally across different spatial and temporal scales, the potential positive feedback of soil microbial respiration in response to climate warming may be less than previously predicted.},
doi = {10.1038/s41467-020-18706-z},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Tue Sep 29 00:00:00 EDT 2020},
month = {Tue Sep 29 00:00:00 EDT 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-020-18706-z
https://doi.org/10.1038/s41467-020-18706-z
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:
Global soil carbon: understanding and managing the largest terrestrial carbon pool
journal, February 2014
- Scharlemann, Jörn PW; Tanner, Edmund VJ; Hiederer, Roland
- Carbon Management, Vol. 5, Issue 1
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
Scientists’ warning to humanity: microorganisms and climate change
journal, June 2019
- Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N.
- Nature Reviews Microbiology, Vol. 17, Issue 9
Temperature sensitivity of soil respiration rates enhanced by microbial community response
journal, September 2014
- Karhu, Kristiina; Auffret, Marc D.; Dungait, Jennifer A. J.
- Nature, Vol. 513, Issue 7516
Global Convergence in the Temperature Sensitivity of Respiration at Ecosystem Level
journal, July 2010
- Mahecha, M. D.; Reichstein, M.; Carvalhais, N.
- Science, Vol. 329, Issue 5993
Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming
journal, February 2016
- Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou
- Nature Climate Change, Vol. 6, Issue 6
Carbon input by roots into the soil: Quantification of rhizodeposition from root to ecosystem scale
journal, September 2017
- Pausch, Johanna; Kuzyakov, Yakov
- Global Change Biology, Vol. 24, Issue 1
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
Climate warming accelerates temporal scaling of grassland soil microbial biodiversity
journal, March 2019
- Guo, Xue; Zhou, Xishu; Hale, Lauren
- Nature Ecology & Evolution, Vol. 3, Issue 4
Underestimates of Grassland Gross Primary Production in MODIS Standard Products
journal, November 2018
- Zhu, Xiaoyan; Pei, Yanyan; Zheng, Zhaopei
- Remote Sensing, Vol. 10, Issue 11
The whole-soil carbon flux in response to warming
journal, March 2017
- Hicks Pries, Caitlin E.; Castanha, C.; Porras, R. C.
- Science, Vol. 355, Issue 6332
Relative information contributions of model vs. data to short- and long-term forecasts of forest carbon dynamics
journal, July 2011
- Weng, Ensheng; Luo, Yiqi
- Ecological Applications, Vol. 21, Issue 5
Community analysis by Biolog: curve integration for statistical analysis of activated sludge microbial habitats
journal, November 1996
- Guckert, James B.; Carr, Gregory J.; Johnson, Troy D.
- Journal of Microbiological Methods, Vol. 27, Issue 2-3
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats
journal, January 2015
- Zhou, Jizhong; He, Zhili; Yang, Yunfeng
- mBio, Vol. 6, Issue 1
Dynamics of labile and recalcitrant soil carbon pools in a sorghum free-air CO2 enrichment (FACE) agroecosystem
journal, September 2007
- Cheng, L.; Leavitt, S. W.; Kimball, B. A.
- Soil Biology and Biochemistry, Vol. 39, Issue 9
Analysis of Factors Controlling Soil Organic Matter Levels in Great Plains Grasslands1
journal, January 1987
- Parton, W. J.; Schimel, D. S.; Cole, C. V.
- Soil Science Society of America Journal, Vol. 51, Issue 5
Model parameterization to represent processes at unresolved scales and changing properties of evolving systems
journal, January 2020
- Luo, Yiqi; Schuur, Edward A. G.
- Global Change Biology, Vol. 26, Issue 3
Concurrent and lagged impacts of an anomalously warm year on autotrophic and heterotrophic components of soil respiration: a deconvolution analysis
journal, April 2010
- Zhou, Xuhui; Luo, Yiqi; Gao, Chao
- New Phytologist, Vol. 187, Issue 1
Reproducibility and quantitation of amplicon sequencing-based detection
journal, February 2011
- Zhou, Jizhong; Wu, Liyou; Deng, Ye
- The ISME Journal, Vol. 5, Issue 8
Thermal adaptation of heterotrophic soil respiration in laboratory microcosms
journal, May 2010
- Bradford, Mark A.; Watts, Brian W.; Davies, Christian A.
- Global Change Biology, Vol. 16, Issue 5
Aboveground Biomass Estimation with the Canopy Intercept Method: A Plant Growth Form Caveat
journal, February 1990
- Frank, Douglas A.; McNaughton, Samuel J.
- Oikos, Vol. 57, Issue 1
Terrestrial Carbon–Cycle Feedback to Climate Warming
journal, December 2007
- Luo, Yiqi
- Annual Review of Ecology, Evolution, and Systematics, Vol. 38, Issue 1
Partitioning soil respiration: quantifying the artifacts of the trenching method
journal, July 2018
- Savage, K. E.; Davidson, E. A.; Abramoff, R. Z.
- Biogeochemistry, Vol. 140, Issue 1
Thermodynamic theory explains the temperature optima of soil microbial processes and high Q 10 values at low temperatures
journal, May 2014
- Schipper, Louis A.; Hobbs, Joanne K.; Rutledge, Susanna
- Global Change Biology, Vol. 20, Issue 11
Boreal and temperate trees show strong acclimation of respiration to warming
journal, March 2016
- Reich, Peter B.; Sendall, Kerrie M.; Stefanski, Artur
- Nature, Vol. 531, Issue 7596
Persistence of soil organic matter as an ecosystem property
journal, October 2011
- Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel
- Nature, Vol. 478, Issue 7367
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
Managing uncertainty in soil carbon feedbacks to climate change
journal, July 2016
- Bradford, Mark A.; Wieder, William R.; Bonan, Gordon B.
- Nature Climate Change, Vol. 6, Issue 8
Lagged effects of experimental warming and doubled precipitation on annual and seasonal aboveground biomass production in a tallgrass prairie
journal, December 2008
- Sherry, Rebecca A.; Weng, Ensheng; Arnone Iii, John A.
- Global Change Biology, Vol. 14, Issue 12
Soil moisture drives microbial controls on carbon decomposition in two subtropical forests
journal, March 2019
- Wang, Gangsheng; Huang, Wenjuan; Mayes, Melanie A.
- Soil Biology and Biochemistry, Vol. 130
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Toward a Metabolic Theory of Ecology
journal, July 2004
- Brown, James H.; Gillooly, James F.; Allen, Andrew P.
- Ecology, Vol. 85, Issue 7
Measuring explained variation in linear mixed effects models
journal, January 2003
- Xu, Ronghui
- Statistics in Medicine, Vol. 22, Issue 22
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
Microbial dormancy improves development and experimental validation of ecosystem model
journal, July 2014
- Wang, Gangsheng; Jagadamma, Sindhu; Mayes, Melanie A.
- The ISME Journal, Vol. 9, Issue 1
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
Biotic responses buffer warming-induced soil organic carbon loss in Arctic tundra
journal, June 2018
- Liang, Junyi; Xia, Jiangyang; Shi, Zheng
- Global Change Biology, Vol. 24, Issue 10
Temperature sensitivity of soil organic carbon decomposition increased with mean carbon residence time: Field incubation and data assimilation
journal, September 2017
- Zhou, Xuhui; Xu, Xia; Zhou, Guiyao
- Global Change Biology, Vol. 24, Issue 2
Temperature sensitivity of soil microbial activity modeled by the square root equation as a unifying model to differentiate between direct temperature effects and microbial community adaptation
journal, May 2018
- Bååth, Erland
- Global Change Biology, Vol. 24, Issue 7
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
Biodiversity increases the resistance of ecosystem productivity to climate extremes
journal, October 2015
- Isbell, Forest; Craven, Dylan; Connolly, John
- Nature, Vol. 526, Issue 7574
Acclimatization of soil respiration to warming in a tall grass prairie
journal, October 2001
- Luo, Yiqi; Wan, Shiqiang; Hui, Dafeng
- Nature, Vol. 413, Issue 6856
Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observations
journal, January 2013
- Todd-Brown, K. E. O.; Randerson, J. T.; Post, W. M.
- Biogeosciences, Vol. 10, Issue 3
Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation
journal, January 2019
- Bradford, Mark A.; McCulley, Rebecca L.; Crowther, Thomas. W.
- Nature Ecology & Evolution, Vol. 3, Issue 2
Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response
journal, August 2007
- Hartley, Iain P.; Heinemeyer, Andreas; Ineson, Phil
- Global Change Biology, Vol. 13, Issue 8
Climate–Carbon Cycle Feedback Analysis: Results from the C 4 MIP Model Intercomparison
journal, July 2006
- Friedlingstein, P.; Cox, P.; Betts, R.
- Journal of Climate, Vol. 19, Issue 14
Plant communities as drivers of soil respiration: pathways, mechanisms, and significance for global change
journal, January 2011
- Metcalfe, D. B.; Fisher, R. A.; Wardle, D. A.
- Biogeosciences, Vol. 8, Issue 8
Changes of labile and recalcitrant carbon pools under nitrogen addition in a city lawn soil
journal, December 2013
- Jiang, Xinyu; Cao, Lixiang; Zhang, Renduo
- Journal of Soils and Sediments, Vol. 14, Issue 3
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
Temperature response of soil respiration largely unaltered with experimental warming
journal, November 2016
- Carey, Joanna C.; Tang, Jianwu; Templer, Pamela H.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models
journal, April 2013
- Moyano, Fernando E.; Manzoni, Stefano; Chenu, Claire
- Soil Biology and Biochemistry, Vol. 59
Terrestrial ecosystem carbon dynamics and climate feedbacks
journal, January 2008
- Heimann, Martin; Reichstein, Markus
- Nature, Vol. 451, Issue 7176
Modeling Global Soil Carbon and Soil Microbial Carbon by Integrating Microbial Processes into the Ecosystem Process Model TRIPLEX-GHG: GLOBAL SOIL CARBON AND MICROBIAL CARBON
journal, October 2017
- Wang, Kefeng; Peng, Changhui; Zhu, Qiuan
- Journal of Advances in Modeling Earth Systems, Vol. 9, Issue 6
Net primary productivity and rain-use efficiency as affected by warming, altered precipitation, and clipping in a mixed-grass prairie
journal, July 2013
- Xu, Xia; Sherry, Rebecca A.; Niu, Shuli
- Global Change Biology, Vol. 19, Issue 9
Integrating microbial ecology into ecosystem models: challenges and priorities
journal, September 2011
- Treseder, Kathleen K.; Balser, Teri C.; Bradford, Mark A.
- Biogeochemistry, Vol. 109, Issue 1-3
Root trenching: a useful tool to estimate autotrophic soil respiration? A case study in an Austrian mountain forest
journal, December 2008
- Díaz-Pinés, Eugenio; Schindlbacher, Andreas; Pfeffer, Michael
- European Journal of Forest Research, Vol. 129, Issue 1
HydroTest: A web-based toolbox of evaluation metrics for the standardised assessment of hydrological forecasts
journal, July 2007
- Dawson, C. W.; Abrahart, R. J.; See, L. M.
- Environmental Modelling & Software, Vol. 22, Issue 7
Shifts in temperature response of soil respiration between adjacent irrigated and non-irrigated grazed pastures
journal, December 2019
- Schipper, Louis A.; Petrie, Olivia J.; O’Neill, Tanya A.
- Agriculture, Ecosystems & Environment, Vol. 285
Effective and efficient global optimization for conceptual rainfall-runoff models
journal, April 1992
- Duan, Qingyun; Sorooshian, Soroosh; Gupta, Vijai
- Water Resources Research, Vol. 28, Issue 4
Climate warming leads to divergent succession of grassland microbial communities
journal, August 2018
- Guo, Xue; Feng, Jiajie; Shi, Zhou
- Nature Climate Change, Vol. 8, Issue 9