Microorganisms drive soil carbon mineralization and changes in their activity with increased temperature could feedback to climate change. Variation in microbial biodiversity and the temperature sensitivities (Q10) of individual taxa may explain differences in the Q10 of soil respiration, a possibility not previously examined due to methodological limitations. Here, we show phylogenetic and taxonomic variation in the Q10 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 Q10, which was strongly predictive of soil respiration Q10 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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Soil respiration, microbial biomass, and figure data are available in the Supplementary materials. Raw sequence data for this study are available in Sequence Read Achieve (SRA) database of NCBI under accession numbers PRJNA649787, PRJNA649546, PRJNA649571, and PRJNA649802.
Code associated with qSIP calculations is publicly available at https://bitbucket.org/QuantitativeSIP/qsip_repo.
Bradford MA, Wieder WR, Bonan GB, Fierer N, Raymond PA, Crowther TW. Managing uncertainty in soil carbon feedbacks to climate change. Nat Clim Chang. 2016;6:751–8.
Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.
Crowther TW, Hoogen JVD, Wan J, Mayes MA, Keiser AD, Mo L, et al. The global soil community and its influence on biogeochemistry. Science. 2019;365:eaav0550.
Heimann M, Reichstein M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature. 2008;451:289–92.
Wieder WR, Bonan GB, Allison SD. Global soil carbon projections are improved by modelling microbial processes. Nat Clim Chang. 2013;3:909–12.
Walker TWN, Kaiser C, Strasser F, Herbold CW, Leblans NIW, Woebken D, et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat Clim Chang. 2018;8:885–9.
Crowther TW, Todd-Brown KEO, Rowe CW, Wieder WR, Carey JC, Machmuller MB, et al. Quantifying global soil carbon losses in response to warming. Nature. 2016;540:104–8.
Li JQ, Pei JM, Pendall E, Fang CM, Nie M. Spatial heterogeneity of temperature sensitivity of soil respiration: a global analysis of field observations. Soil Biol Biochem. 2020;141:107675.
Wang QK, Zhao XC, Chen LC, Yang QP, Chen S, Zhang WD, et al. Global synthesis of temperature sensitivity of soil organic carbon decomposition: latitudinal patterns and mechanisms. Funct Ecol. 2019;33:514–23.
Nottingham AT, Baath E, Reischke S, Salinas N, Meir P. Adaptation of soil microbial growth to temperature: using a tropical elevation gradient to predict future changes. Glob Chang Biol. 2019;25:827–38.
Ye JS, Bradford MA, Dacal M, Maestre FT, García-Palacios P. Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally. Glob Chang Biol. 2019;25:3354–64.
Smith TP, Thomas TJH, Garcia-Carreras B, Sal S, Yvon-Durocher G, Bell T, et al. Community-level respiration of prokaryotic microbes may rise with global warming. Nat Commun. 2019;10:5124.
Schipper LA, Hobbs JK, Rutledge S, Arcus VL. Thermodynamic theory explains the temperature optima of soil microbial processes and high Q10 values at low temperatures. Glob Chang Biol 2014;20:3578–86.
Pietikainen J, Pettersson M, Baath E. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol. 2005;52:49–58.
Bárcenas-Moreno G, Gómez-Brandón M, Rousk J, Bååth E. Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob Chang Biol. 2009;15:2950–7.
Engqvist MKM. Correlating enzyme annotations with a large set of microbial growth temperatures reveals metabolic adaptations to growth at diverse temperatures. BMC Microbiol. 2018;18:177.
Oliverio AM, Bradford MA, Fierer N. Identifying the microbial taxa that consistently respond to soil warming across time and space. Glob Chang Biol. 2017;23:2117–29.
Bier RL, Bernhardt ES, Boot CM, Graham EB, Hall EK, Lennon JT, et al. Linking microbial community structure and microbial processes: an empirical and conceptual overview. FEMS Microbiol Ecol. 2015;91:fiv113.
Dubey A, Malla MA, Khan F, Chowdhary K, Yadav S, Kumar A, et al. Soil microbiome: a key player for conservation of soil health under changing climate. Biodivers Conserv. 2019;28:2405–29.
Hungate BA, Mau RL, Schwartz E, Caporaso JG, Dijkstra P, van Gestel N, et al. Quantitative microbial ecology through stable isotope probing. Appl Environ Microbiol. 2015;81:7570–81.
Koch BJ, McHugh TA, Hayer M, Schwartz E, Blazewicz SJ, Dijkstra P, et al. Estimating taxon-specific population dynamics in diverse microbial communities. Ecosphere. 2018;9:e02090.
Hamdi S, Moyano F, Sall S, Bernoux M, Chevallier T. Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions. Soil Biol Biochem. 2013;58:115–26.
Martiny AC, Treseder K, Pusch G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 2013;7:830–8.
DeAngelis KM, Pold G, Topçuoğlu BD, van Diepen LTA, Varney RM, Blanchard JL, et al. Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol. 2015;6:104.
Euskirchen ES, Bret-Harte MS, Shaver GR, Edgar CW, Romanovsky VE. Long-term release of carbon dioxide from Arctic Tundra ecosystems in Alaska. Ecosystems. 2017;20:960–74.
Reed SC, Reibold R, Cavaleri MA, Alonso-Rodríguez AM, Berberich ME, Wood TE. Chapter six—soil biogeochemical responses of a tropical forest to warming and hurricane disturbance. In: Dumbrell AJ, Turner EC, Fayle TM, editors. Advances in ecological research. (Academic Press, Cambridge MA, 2020) pp 225–52.
Witt C, Gaunt JL, Galicia CC, Ottow JCG, Neue HU. A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biol Fertil Soils. 2000;30:510–9.
Berry D, Ben Mahfoudh K, Wagner M, Loy A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol. 2012;78:612.
Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Micro Ecol. 2015;75:129–37.
Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.
Rohland N, Reich D. Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res. 2012;22:939–46.
Aronesty E. ea-utils: “Command-line tools for processing biological sequencing data”. 2011. https://github.com/ExpressionAnalysis/ea-utils.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Caporaso JG, Bittinger K, Bushman FD, Desantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26:266–7.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10:57–9.
Morrissey EM, Mau RL, Schwartz E, McHugh TA, Dijkstra P, Koch BJ, et al. Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter. ISME J. 2017;11:1890–9.
Li J, Mau RL, Dijkstra P, Koch BJ, Schwartz E, Liu X-JA, et al. Predictive genomic traits for bacterial growth in culture versus actual growth in soil. ISME J. 2019;13:2162–72.
Gross N, Bagousse-Pinguet YL, Liancourt P, Berdugo M, Gotelli NJ, Maestre FT. Functional trait diversity maximizes ecosystem multifunctionality. Nat Ecol Evol. 2017;1:0132.
Laliberté E, Norton DA, Scott D. Contrasting effects of productivity and disturbance on plant functional diversity at local and metacommunity scales. J Veg Sci. 2013;24:834–42.
Plass-Johnson JG, Taylor MH, Husain AAA, Teichberg MC, Ferse SCA. Non-random variability in functional composition of coral reef fish communities along an environmental gradient. PLOS ONE. 2016;11:e0154014.
Götzenberger L, Botta-Dukát Z, Lepš J, Pärtel M, Zobel M, de Bello F. Which randomizations detect convergence and divergence in trait-based community assembly? A test of commonly used null models. J Veg Sci. 2016;27:1275–87.
Delgado-Baquerizo M, Trivedi P, Trivedi C, Eldridge DJ, Reich PB, Jeffries TC, et al. Microbial richness and composition independently drive soil multifunctionality. Funct Ecol. 2017;31:2330–43.
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. https://www.R-project.org/.
Bruelheide H, Dengler J, Purschke O, Lenoir J, Jiménez-Alfaro B, Hennekens SM, et al. Global trait–environment relationships of plant communities. Nat Ecol Evol. 2018;2:1906–17.
Piton G, Legay N, Arnoldi C, Lavorel S, Clément J-C, Foulquier A. 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. J Ecol. 2020;108:876–93.
Alster CJ, von Fischer JC, Allison SD, Treseder KK. Embracing a new paradigm for temperature sensitivity of soil microbes. Glob Chang Biol. 2020;26:3221–9.
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.
Li J, Nie M, Pendall E, Reich PB, Pei J, Noh NJ, et al. Biogeographic variation in temperature sensitivity of decomposition in forest soils. Glob Chang Biol. 2020;26:1873–85.
Lipson DA. The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front Microbiol. 2015;6:615.
Buckeridge KM, Mason KE, McNamara NP, Ostle N, Puissant J, Goodall T, et al. Environmental and microbial controls on microbial necromass recycling, an important precursor for soil carbon stabilization. Commun Earth Environ. 2020;1:36.
Ali A, Yan E-R, Chang SX, Cheng J-Y, Liu X-Y. Community-weighted mean of leaf traits and divergence of wood traits predict aboveground biomass in secondary subtropical forests. Sci Total Environ. 2017;574:654–62.
Buzzard V, Michaletz ST, Deng Y, He Z, Ning D, Shen L, et al. Continental scale structuring of forest and soil diversity via functional traits. Nat Ecol Evol. 2019;3:1298–308.
Luo Y-H, Cadotte MW, Burgess KS, Liu J, Tan S-L, Zou J-Y, et al. Greater than the sum of the parts: how the species composition in different forest strata influence ecosystem function. Ecol Lett. 2019;22:1449–61.
Díaz S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM. Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci USA. 2007;104:20684–9.
Bradford MA. Thermal adaptation of decomposer communities in warming soils. Front Microbiol. 2013;4:333.
Morrissey EM, Mau RL, Schwartz E, Koch BJ, Hayer M, Hungate BA. Taxonomic patterns in the nitrogen assimilation of soil prokaryotes. Environ Microbiol. 2018;20:1112–9.
Coskun OK, Ozen V, Wankel SD, Orsi WD. Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O. ISME J. 2019;13:1546–59.
Zhou G, Zhou X, Liu R, Du Z, Zhou L, Li S, et al. Soil fungi and fine root biomass mediate drought-induced reductions in soil respiration. Funct Ecol. 2020;34:2634–43.
Melillo JM, Frey SD, Deangelis KM, Werner WJ, Bernard MJ, Bowles FP, et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science. 2017;358:101–5.
Johnston ASA, Sibly RM. The influence of soil communities on the temperature sensitivity of soil respiration. Nat Ecol Evol. 2018;2:1597–602.
This work was supported by the U.S. Department of Energy, Program in Genomic Sciences (DE-SC0020172 and DE-SC0016207). Work at LLNL was performed under the auspices of the U.S. Department of Energy under Contract DE-AC52-07NA27344 and Awards SCW1590 and SCW1679. CW acknowledges the funding of Key Research Program of Frontier Sciences, CAS (ZDBS-LY-DQC019), Youth Innovation Promotion Association CAS to CW (2018231), and CAS scholarship.
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Wang, C., Morrissey, E.M., Mau, R.L. et al. The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization. ISME J (2021). https://doi.org/10.1038/s41396-021-00959-1