The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization

Wang, Chao; Morrissey, Ember M.; Mau, Rebecca L.; Hayer, Michaela; Piñeiro, Juan; Mack, Michelle C.; Marks, Jane C.; Bell, Sheryl L.; Miller, Samantha N.; Schwartz, Egbert; Dijkstra, Paul; Koch, Benjamin J.; Stone, Bram W.; Purcell, Alicia M.; Blazewicz, Steven J.; Hofmockel, Kirsten S.; Pett-Ridge, Jennifer; Hungate, Bruce A.

doi:10.1038/s41396-021-00959-1

Title: The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization

Journal Article · Mon Mar 29 00:00:00 EDT 2021 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-021-00959-1· OSTI ID:1813712

^[1];

^[2]; Mau, Rebecca L. ^[3]; Hayer, Michaela ^[3]; Piñeiro, Juan ^[2]; Mack, Michelle C. ^[3]; Marks, Jane C. ^[3];

^[4]; Miller, Samantha N. ^[3]; Schwartz, Egbert ^[3]; Dijkstra, Paul ^[3]; Koch, Benjamin J. ^[3]; Stone, Bram W. ^[3]; Purcell, Alicia M. ^[3]; Blazewicz, Steven J. ^[4];

^[5];

^[4];

^[3]

West Virginia Univ., Morgantown, WV (United States); Chinese Academy of Sciences (CAS), Shenyang, Liaoning (China)
West Virginia Univ., Morgantown, WV (United States)
Northern Arizona Univ., Flagstaff, AZ (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Iowa State Univ., Ames, IA (United States)

Microorganisms drive soil carbon mineralization and changes in their activity with increased temperature could feedback to climate change. Further, variation in microbial biodiversity and the temperature sensitivities ($$Q_{10}$$) of individual taxa may explain differences in the $$Q_{10}$$ of soil respiration, a possibility not previously examined due to methodological limitations. Here, we show phylogenetic and taxonomic variation in the $$Q_{10}$$ of growth (5–35 °C) among soil bacteria from four sites, one from each of Arctic, boreal, temperate, and tropical biomes. Differences in the temperature sensitivities of taxa and the taxonomic composition of communities determined community-assembled bacterial growth $$Q_{10}$$, which was strongly predictive of soil respiration $$Q_{10}$$ within and across biomes. Our results suggest community-assembled traits of microbial taxa may enable enhanced prediction of carbon cycling feedbacks to climate change in ecosystems across the globe.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); Chinese Academy of Sciences (CAS)

DOE Contract Number:: AC52-07NA27344; SC0020172; SC0016207; SCW1590; SCW1679

OSTI ID:: 1813712

Report Number(s):: LLNL-JRNL-813918; 1021365

Journal Information:: The ISME Journal, Vol. 15, Issue 9; ISSN 1751-7362

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

References (58)

Scientists’ warning to humanity: microorganisms and climate change Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N. Nature Reviews Microbiology, Vol. 17, Issue 9 https://doi.org/10.1038/s41579-019-0222-5	journal	June 2019
Microbial temperature sensitivity and biomass change explain soil carbon loss with warming Walker, Tom W. N.; Kaiser, Christina; Strasser, Florian Nature Climate Change, Vol. 8, Issue 10 https://doi.org/10.1038/s41558-018-0259-x	journal	September 2018
Adaptation of soil microbial growth to temperature: Using a tropical elevation gradient to predict future changes Nottingham, Andrew T.; Bååth, Erland; Reischke, Stephanie Global Change Biology, Vol. 25, Issue 3 https://doi.org/10.1111/gcb.14502	journal	January 2019
A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils Witt, C.; Gaunt, J. L.; Galicia, C. C. Biology and Fertility of Soils, Vol. 30, Issue 5-6 https://doi.org/10.1007/s003740050030	journal	March 2000
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment: TEMPERATURE ADAPTATION OF SOIL MICROORGANISMS BÁRcenas-Moreno, Gema; GÓMez-BrandÓN, Maria; Rousk, Johannes Global Change Biology, Vol. 15, Issue 12 https://doi.org/10.1111/j.1365-2486.2009.01882.x	journal	February 2009
Correlating enzyme annotations with a large set of microbial growth temperatures reveals metabolic adaptations to growth at diverse temperatures Engqvist, Martin K. M. BMC Microbiology, Vol. 18, Issue 1 https://doi.org/10.1186/s12866-018-1320-7	journal	November 2018
Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands Piton, Gabin; Legay, Nicolas; Arnoldi, Cindy Journal of Ecology, Vol. 108, Issue 3 https://doi.org/10.1111/1365-2745.13327	journal	January 2020
Global synthesis of temperature sensitivity of soil organic carbon decomposition: Latitudinal patterns and mechanisms Wang, Qingkui; Zhao, Xuechao; Chen, Longchi Functional Ecology, Vol. 33, Issue 3 https://doi.org/10.1111/1365-2435.13256	journal	December 2018
Taxonomic patterns in the nitrogen assimilation of soil prokaryotes: Nitrogen assimilation of soil prokaryotes Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert Environmental Microbiology, Vol. 20, Issue 3 https://doi.org/10.1111/1462-2920.14051	journal	March 2018
Contrasting effects of productivity and disturbance on plant functional diversity at local and metacommunity scales Laliberté, Etienne; Norton, David A.; Scott, David Journal of Vegetation Science, Vol. 24, Issue 5 https://doi.org/10.1111/jvs.12044	journal	January 2013
Soil microbiome: a key player for conservation of soil health under changing climate Dubey, Anamika; Malla, Muneer Ahmad; Khan, Farhat Biodiversity and Conservation, Vol. 28, Issue 8-9 https://doi.org/10.1007/s10531-019-01760-5	journal	April 2019
Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J. Nature Methods, Vol. 10, Issue 1 https://doi.org/10.1038/nmeth.2276	journal	December 2012
Microbial richness and composition independently drive soil multifunctionality Delgado-Baquerizo, Manuel; Trivedi, Pankaj; Trivedi, Chanda Functional Ecology, Vol. 31, Issue 12 https://doi.org/10.1111/1365-2435.12924	journal	July 2017
Non-Random Variability in Functional Composition of Coral Reef Fish Communities along an Environmental Gradient Plass-Johnson, Jeremiah G.; Taylor, Marc H.; Husain, Aidah A. A. PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0154014	journal	April 2016
Greater than the sum of the parts: how the species composition in different forest strata influence ecosystem function Luo, Ya‐Huang; Cadotte, Marc W.; Burgess, Kevin S. Ecology Letters, Vol. 22, Issue 9 https://doi.org/10.1111/ele.13330	journal	July 2019
Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally Ye, Jian‐Sheng; Bradford, Mark A.; Dacal, Marina Global Change Biology, Vol. 25, Issue 10 https://doi.org/10.1111/gcb.14738	journal	July 2019
Environmental and microbial controls on microbial necromass recycling, an important precursor for soil carbon stabilization Buckeridge, Kate M.; Mason, Kelly E.; McNamara, Niall P. Communications Earth & Environment, Vol. 1, Issue 1 https://doi.org/10.1038/s43247-020-00031-4	journal	October 2020
Comparison of temperature effects on soil respiration and bacterial and fungal growth rates PietikÃ¥inen, Janna; Pettersson, Marie; BÃ¥Ã¥th, Erland FEMS Microbiology Ecology, Vol. 52, Issue 1 https://doi.org/10.1016/j.femsec.2004.10.002	journal	March 2005
Quantifying global soil carbon losses in response to warming Crowther, T. W.; Todd-Brown, K. E. O.; Rowe, C. W. Nature, Vol. 540, Issue 7631 https://doi.org/10.1038/nature20150	journal	November 2016
Thermodynamic theory explains the temperature optima of soil microbial processes and high Q ₁₀ values at low temperatures Schipper, Louis A.; Hobbs, Joanne K.; Rutledge, Susanna Global Change Biology, Vol. 20, Issue 11 https://doi.org/10.1111/gcb.12596	journal	May 2014
Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions Hamdi, Salwa; Moyano, Fernando; Sall, Saidou Soil Biology and Biochemistry, Vol. 58 https://doi.org/10.1016/j.soilbio.2012.11.012	journal	March 2013
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton Apprill, A.; McNally, S.; Parsons, R. Aquatic Microbial Ecology, Vol. 75, Issue 2 https://doi.org/10.3354/ame01753	journal	June 2015
Phylogenetic conservatism of functional traits in microorganisms Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.160	journal	December 2012
Estimating taxon‐specific population dynamics in diverse microbial communities Koch, Benjamin J.; McHugh, Theresa A.; Hayer, Michaela Ecosphere, Vol. 9, Issue 1 https://doi.org/10.1002/ecs2.2090	journal	January 2018
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world Melillo, J. M.; Frey, S. D.; DeAngelis, K. M. Science, Vol. 358, Issue 6359 https://doi.org/10.1126/science.aan2874	journal	October 2017
Managing uncertainty in soil carbon feedbacks to climate change Bradford, Mark A.; Wieder, William R.; Bonan, Gordon B. Nature Climate Change, Vol. 6, Issue 8 https://doi.org/10.1038/nclimate3071	journal	July 2016
Which randomizations detect convergence and divergence in trait-based community assembly? A test of commonly used null models Götzenberger, Lars; Botta-Dukát, Zoltán; Lepš, Jan Journal of Vegetation Science, Vol. 27, Issue 6 https://doi.org/10.1111/jvs.12452	journal	August 2016
Community-level respiration of prokaryotic microbes may rise with global warming Smith, Thomas P.; Thomas, Thomas J. H.; García-Carreras, Bernardo Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13109-1	journal	November 2019
Quantitative Microbial Ecology through Stable Isotope Probing Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 81, Issue 21 https://doi.org/10.1128/AEM.02280-15	journal	August 2015
Community-weighted mean of leaf traits and divergence of wood traits predict aboveground biomass in secondary subtropical forests Ali, Arshad; Yan, En-Rong; Chang, Scott X. Science of The Total Environment, Vol. 574 https://doi.org/10.1016/j.scitotenv.2016.09.022	journal	January 2017
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.43	journal	April 2017
Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O Coskun, Ömer K.; Özen, Volkan; Wankel, Scott D. The ISME Journal, Vol. 13, Issue 6 https://doi.org/10.1038/s41396-019-0373-4	journal	February 2019
Identifying the microbial taxa that consistently respond to soil warming across time and space Oliverio, Angela M.; Bradford, Mark A.; Fierer, Noah Global Change Biology, Vol. 23, Issue 5 https://doi.org/10.1111/gcb.13557	journal	November 2016
Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture Rohland, N.; Reich, D. Genome Research, Vol. 22, Issue 5 https://doi.org/10.1101/gr.128124.111	journal	January 2012
Continental scale structuring of forest and soil diversity via functional traits Buzzard, Vanessa; Michaletz, Sean T.; Deng, Ye Nature Ecology & Evolution, Vol. 3, Issue 9 https://doi.org/10.1038/s41559-019-0954-7	journal	August 2019
Global soil carbon projections are improved by modelling microbial processes Wieder, William R.; Bonan, Gordon B.; Allison, Steven D. Nature Climate Change, Vol. 3, Issue 10 https://doi.org/10.1038/nclimate1951	journal	July 2013
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Embracing a new paradigm for temperature sensitivity of soil microbes Alster, Charlotte J.; Fischer, Joseph C.; Allison, Steven D. Global Change Biology, Vol. 26, Issue 6 https://doi.org/10.1111/gcb.15053	journal	March 2020
Linking microbial community structure and microbial processes: an empirical and conceptual overview Bier, Raven L.; Bernhardt, Emily S.; Boot, Claudia M. FEMS Microbiology Ecology, Vol. 91, Issue 10 https://doi.org/10.1093/femsec/fiv113	journal	September 2015
Global trait–environment relationships of plant communities Bruelheide, Helge; Dengler, Jürgen; Purschke, Oliver Nature Ecology & Evolution, Vol. 2, Issue 12 https://doi.org/10.1038/s41559-018-0699-8	journal	November 2018
Functional trait diversity maximizes ecosystem multifunctionality Gross, Nicolas; Bagousse-Pinguet, Yoann Le; Liancourt, Pierre Nature Ecology & Evolution, Vol. 1, Issue 5 https://doi.org/10.1038/s41559-017-0132	journal	April 2017
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Soil fungi and fine root biomass mediate drought‐induced reductions in soil respiration Zhou, Guiyao; Zhou, Xuhui; Liu, Ruiqiang Functional Ecology, Vol. 34, Issue 12 https://doi.org/10.1111/1365-2435.13677	journal	October 2020
Biogeographic variation in temperature sensitivity of decomposition in forest soils Li, Jinquan; Nie, Ming; Pendall, Elise Global Change Biology, Vol. 26, Issue 3 https://doi.org/10.1111/gcb.14838	journal	October 2019
Long-term forest soil warming alters microbial communities in temperate forest soils DeAngelis, Kristen M.; Pold, Grace; TopÃ§uoÄŸlu, BegÃ¼m D. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00104	journal	February 2015
Soil biogeochemical responses of a tropical forest to warming and hurricane disturbance Reed, Sasha C.; Reibold, Robin; Cavaleri, Molly A. Advances in Ecological Research https://doi.org/10.1016/bs.aecr.2020.01.007	book	March 2020
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification Berry, David; Ben Mahfoudh, Karim; Wagner, Michael Applied and Environmental Microbiology, Vol. 78, Issue 2 https://doi.org/10.1128/AEM.07448-11	journal	December 2011
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
Thermal adaptation of decomposer communities in warming soils Bradford, Mark A. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00333	journal	January 2013
Incorporating plant functional diversity effects in ecosystem service assessments Diaz, S.; Lavorel, S.; de Bello, F. Proceedings of the National Academy of Sciences, Vol. 104, Issue 52 https://doi.org/10.1073/pnas.0704716104	journal	December 2007
Terrestrial ecosystem carbon dynamics and climate feedbacks Heimann, Martin; Reichstein, Markus Nature, Vol. 451, Issue 7176 https://doi.org/10.1038/nature06591	journal	January 2008
The influence of soil communities on the temperature sensitivity of soil respiration Johnston, Alice S. A.; Sibly, Richard M. Nature Ecology & Evolution, Vol. 2, Issue 10 https://doi.org/10.1038/s41559-018-0648-6	journal	August 2018
Spatial heterogeneity of temperature sensitivity of soil respiration: A global analysis of field observations Li, Jinquan; Pei, Junmin; Pendall, Elise Soil Biology and Biochemistry, Vol. 141 https://doi.org/10.1016/j.soilbio.2019.107675	journal	February 2020
Long-Term Release of Carbon Dioxide from Arctic Tundra Ecosystems in Alaska Euskirchen, E. S.; Bret-Harte, M. S.; Shaver, G. R. Ecosystems, Vol. 20, Issue 5 https://doi.org/10.1007/s10021-016-0085-9	journal	November 2016
Predictive genomic traits for bacterial growth in culture versus actual growth in soil Li, Junhui; Mau, Rebecca L.; Dijkstra, Paul The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0422-z	journal	May 2019
The global soil community and its influence on biogeochemistry Crowther, T. W.; van den Hoogen, J.; Wan, J. Science, Vol. 365, Issue 6455 https://doi.org/10.1126/science.aav0550	journal	August 2019

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