Anthropogenic warming is expected to accelerate global soil organic carbon (SOC) losses via microbial decomposition, yet, there is still no consensus on the loss magnitude. In this Perspective, we argue that, despite the mechanistic uncertainty underlying these losses, there is confidence that a strong, positive land carbon–climate feedback can be expected. Two major lines of evidence support net global SOC losses with warming via increases in soil microbial metabolic activity: the increase in soil respiration with temperature and the accumulation of SOC in low mean annual temperature regions. Warming-induced SOC losses are likely to be of a magnitude relevant for emission negotiations and necessitate more aggressive emission reduction targets to limit climate change to 1.5 °C by 2100. We suggest that microbial community–temperature interactions, and how they are influenced by substrate availability, are promising research areas to improve the accuracy and precision of the magnitude estimates of projected SOC losses.
Your institute does not have access to this article
Open Access articles citing this article.
Nature Communications Open Access 20 July 2022
Unexpected microbial metabolic responses to elevated temperatures and nitrogen addition in subarctic soils under different land uses
Biogeochemistry Open Access 17 June 2022
Nature Communications Open Access 18 November 2021
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Jackson, R. B. et al. The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu. Rev. Ecol. Evol. Syst. 48, 419–445 (2017).
Köchy, M., Hiederer, R. & Freibauer, A. Global distribution of soil organic carbon – Part 1: Masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wetlands, and the world. Soil 1, 351–365 (2015).
Le Quéré, C. et al. Global carbon budget 2013. Earth Syst. Sci. Data 6, 235–263 (2014).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).
Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).
Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).
Intergovernmental Panel on Climate Change (IPCC). Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2013).
Wieder, W. R., Sulman, B. N., Hartman, M. D., Koven, C. D. & Bradford, M. A. Arctic soil governs whether climate change drives global losses or gains in soil carbon. Geophys. Res. Lett. 46, 14486–14495 (2019).
Guo, X. et al. Gene-informed decomposition model predicts lower soil carbon loss due to persistent microbial adaptation to warming. Nat. Commun. 11, 4897 (2020).
Friedlingstein, P. et al. Climate–carbon cycle feedback analysis: results from the C4MIP model intercomparison. J. Clim. 19, 3337–3353 (2006).
Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Chang. 6, 791–795 (2016).
Keenan, T. F. & Riley, W. J. Greening of the land surface in the world’s cold regions consistent with recent warming. Nat. Clim. Chang. 8, 825–828 (2018).
Euskirchen, E. S., Mcguire, A. D., Chapin, F. S., Yi, S. & Thompson, C. C. Changes in vegetation in northern Alaska under scenarios of climate change, 2003–2100: implications for climate feedbacks. Ecol. Appl. 19, 1022–1043 (2009).
Conant, R. T. et al. Temperature and soil organic matter decomposition rates – synthesis of current knowledge and a way forward. Glob. Chang. Biol. 17, 3392–3404 (2011).
Peñuelas, J. et al. Shifting from a fertilization-dominated to a warming-dominated period. Nat. Ecol. Evol. 1, 1438–1445 (2017).
Naidu, D. G. & Bagchi, S. Greening of the earth does not compensate for rising soil heterotrophic respiration under climate change. Glob. Chang. Biol. 27, 2029–2038 (2021).
Koven, C. D., Lawrence, D. M. & Riley, W. J. Permafrost carbon–climate feedback is sensitive to deep soil carbon decomposability but not deep soil nitrogen dynamics. Proc. Natl Acad. Sci. USA 112, 3752–3757 (2015).
Xu, X. et al. Plant community structure regulates responses of prairie soil respiration to decadal experimental warming. Glob. Chang. Biol. 21, 3846–3853 (2015).
Melillo, J. M. et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105 (2017).
Guo, X. et al. Climate warming leads to divergent succession of grassland microbial communities. Nat. Clim. Chang. 8, 813–818 (2018).
Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Chang. 2, 106–110 (2012).
Luo, Y., Wan, S., Hui, D. & Wallace, L. L. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413, 622–625 (2001).
García-Palacios, P. et al. Pathways regulating decreased soil respiration with warming in a biocrust-dominated dryland. Glob. Chang. Biol. 24, 4645–4656 (2018).
Karhu, K. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014).
Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).
Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).
Crowther, T. W. & Bradford, M. A. Thermal acclimation in widespread heterotrophic soil microbes. Ecol. Lett. 16, 469–477 (2013).
Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Chang. 3, 909–912 (2013).
Mueller, C. W. et al. Large amounts of labile organic carbon in permafrost soils of northern Alaska. Glob. Chang. Biol. 21, 2804–2817 (2015).
Poeplau, C., Kätterer, T., Leblans, N. I. W. & Sigurdsson, B. D. Sensitivity of soil carbon fractions and their specific stabilization mechanisms to extreme soil warming in a subarctic grassland. Glob. Chang. Biol. 23, 1316–1327 (2017).
Wang, X. et al. Soil respiration under climate warming: Differential response of heterotrophic and autotrophic respiration. Glob. Chang. Biol. 20, 3229–3237 (2014).
Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 13797–13802 (2016).
Crowther, T. W. et al. The global soil community and its influence on biogeochemistry. Science 365, eaav0550 (2019).
Raich, J. W. & Schlesinger, W. The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44, 81–99 (1992).
Jian, J. et al. A restructured and updated global soil respiration database (SRDB-V5). Earth Syst. Sci. Data 13, 255–267 (2021).
Bond-Lamberty, B. & Thomson, A. A global database of soil respiration data. Biogeosciences 7, 1915–1926 (2010).
Rustad, L. E., Huntington, T. G. & Boone, R. D. Controls on soil respiration: Implications for climate change. Biogeochemistry 48, 1–6 (2000).
Hursh, A. et al. The sensitivity of soil respiration to soil temperature, moisture, and carbon supply at the global scale. Glob. Chang. Biol. 23, 2090–2103 (2017).
Xue, K. et al. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. Nat. Clim. Chang. 6, 595–600 (2016).
Hengl, T. et al. SoilGrids250m: Global gridded soil information based on machine learning. PLoS One 12, e0169748 (2017).
Ballantyne, A. et al. Accelerating net terrestrial carbon uptake during the warming hiatus due to reduced respiration. Nat. Clim. Chang. 7, 148–152 (2017).
Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).
Shi, Z. et al. The age distribution of global soil carbon inferred from radiocarbon measurements. Nat. Geosci. 13, 555–559 (2020).
Raich, J. W., Russell, A. E., Kitayama, K., Parton, W. & Vitousek, P. M. Temperature influences carbon accumulation in moist tropical forests. Ecology 87, 76–87 (2006).
Parton, W. J., Stewart, J. W. B. & Cole, C. V. Dynamics of C, N, P and S in grassland soils: a model. Biogeochemistry 5, 109–131 (1988).
Plaza, C. et al. Direct observation of permafrost degradation and rapid soil carbon loss in tundra. Nat. Geosci. 12, 627–631 (2019).
Koven, C. D., Hugelius, G., Lawrence, D. M. & Wieder, W. R. Higher climatological temperature sensitivity of soil carbon in cold than warm climates. Nat. Clim. Chang. 7, 817–822 (2017).
Kirschbaum, M. U. F. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol. Biochem. 27, 753–760 (1995).
Kirschbaum, M. U. F. The temperature dependence of organic-matter decomposition—still a topic of debate. Soil Biol. Biochem. 38, 2510–2518 (2006).
Serreze, M. C. & Barry, R. G. Processes and impacts of Arctic amplification: A research synthesis. Glob. Planet. Change 77, 85–96 (2011).
Serna-Chavez, H. M., Fierer, N. & Van Bodegom, P. M. Global drivers and patterns of microbial abundance in soil. Glob. Ecol. Biogeogr. 22, 1162–1172 (2013).
Xu, X. et al. Global pattern and controls of soil microbial metabolic quotient. Ecol. Monogr. 87, 429–441 (2017).
van den Hoogen, J. et al. Soil nematode abundance and functional group composition at a global scale. Nature 572, 194–198 (2019).
Hashimoto, S. et al. Global spatiotemporal distribution of soil respiration modeled using a global database. Biogeosciences 12, 4121–4132 (2015).
Buchkowski, R. W., Bradford, M. A., Grandy, A. S., Schmitz, O. J. & Wieder, W. R. Applying population and community ecology theory to advance understanding of belowground biogeochemistry. Ecol. Lett. 20, 231–245 (2017).
Bradford, M. A. et al. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Chang. 6, 751–758 (2016).
Trivedi, P., Anderson, I. C. & Singh, B. K. Microbial modulators of soil carbon storage: Integrating genomic and metabolic knowledge for global prediction. Trends Microbiol. 21, 641–651 (2013).
Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).
Hutchins, D. A. et al. Climate change microbiology — problems and perspectives. Nat. Rev. Microbiol. 17, 391–396 (2019).
Hartley, I. P., Hopkins, D. W., Garnett, M. H., Sommerkorn, M. & Wookey, P. A. Soil microbial respiration in arctic soil does not acclimate to temperature. Ecol. Lett. 11, 1092–1100 (2008).
Bradford, M. A. et al. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nat. Ecol. Evol. 3, 223–231 (2019).
Dacal, M., Bradford, M. A., Plaza, C., Maestre, F. T. & García-Palacios, P. Soil microbial respiration adapts to ambient temperature in global drylands. Nat. Ecol. Evol. 3, 232–238 (2019).
Sierra, C. A., Trumbore, S. E., Davidson, E. A., Vicca, S. & Janssens, I. Sensitivity of decomposition rates of soil organic matter with respect to simultaneous changes in temperature and moisture. J. Adv. Model. Earth Syst. 7, 335–356 (2015).
Birgander, J., Reischke, S., Jones, D. L. & Rousk, J. Temperature adaptation of bacterial growth and 14C-glucose mineralisation in a laboratory study. Soil Biol. Biochem. 65, 294–303 (2013).
Sokol, N. W., Sanderman, J. & Bradford, M. A. Pathways of mineral-associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry. Glob. Chang. Biol. 25, 12–24 (2019).
Bradford, M. A. Thermal adaptation of decomposer communities in warming soils. Front. Microbiol. 4, 333 (2013).
Walker, T. W. N. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Chang. 8, 885–889 (2018).
Tucker, C. L., Bell, J., Pendall, E. & Ogle, K. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob. Chang. Biol. 19, 252–263 (2013).
Takriti, M. et al. Soil organic matter quality exerts a stronger control than stoichiometry on microbial substrate use efficiency along a latitudinal transect. Soil Biol. Biochem. 121, 212–220 (2018).
Frey, S. D., Lee, J., Melillo, J. M. & Six, J. The temperature response of soil microbial efficiency and its feedback to climate. Nat. Clim. Chang. 3, 395–398 (2013).
Alster, C. J., von Fischer, J. C., Allison, S. D. & Treseder, K. K. Embracing a new paradigm for temperature sensitivity of soil microbes. Glob. Chang. Biol. 26, 3221–3229 (2020).
Bååth, E. 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. Glob. Chang. Biol. 24, 2850–2861 (2018).
Ratkowsky, D. A., Olley, J., McMeekin, T. A. & Ball, A. Relationship between temperature and growth rate of bacterial cultures. J. Bacteriol. 149, 1–5 (1982).
Rinnan, R., Rousk, J., Yergeau, E., Kowalchuk, G. A. & Bååth, E. Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Glob. Chang. Biol. 15, 2615–2625 (2009).
Roller, B. R. K. & Schmidt, T. M. The physiology and ecological implications of efficient growth. ISME J. 9, 1481–1487 (2015).
Rousk, J., Frey, S. D. & Bååth, E. Temperature adaptation of bacterial communities in experimentally warmed forest soils. Glob. Chang. Biol. 18, 3252–3258 (2012).
Coleman, K. et al. Simulating trends in soil organic carbon in long-term experiments using RothC-26.3. Geoderma 81, 29–44 (1997).
Treseder, K. K. et al. Integrating microbial ecology into ecosystem models: Challenges and priorities. Biogeochemistry 109, 7–18 (2012).
Hagerty, S. B. et al. Accelerated microbial turnover but constant growth efficiency with warming in soil. Nat. Clim. Chang. 4, 903–906 (2014).
Steinweg, J. M., Plante, A. F., Conant, R. T., Paul, E. A. & Tanaka, D. L. Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biol. Biochem. 40, 2722–2728 (2008).
Sinsabaugh, R. L. et al. Stoichiometry of microbial carbon use efficiency in soils. Ecol. Monogr. 86, 172–189 (2016).
Ye, J.-S., Bradford, M. A., Dacal, M., Maestre, F. T. & García-Palacios, P. Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally. Glob. Chang. Biol. 25, 3354–3364 (2019).
Ye, J. S., Bradford, M. A., Maestre, F. T., Li, F. M. & García-Palacios, P. Compensatory thermal adaptation of soil microbial respiration rates in global croplands. Glob. Biogeochem. Cycles 34, e2019GB006507 (2020).
Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).
Hartley, I. P., Heinemeyer, A. & Ineson, P. Effects of three years of soil warming and shading on the rate of soil respiration: Substrate availability and not thermal acclimation mediates observed response. Glob. Chang. Biol. 13, 1761–1770 (2007).
Hopkins, F. M., Torn, M. S. & Trumbore, S. E. Warming accelerates decomposition of decades-old carbon in forest soils. Proc. Natl Acad. Sci. USA 109, 1753–1751 (2012).
Feng, W. et al. Enhanced decomposition of stable soil organic carbon and microbial catabolic potentials by long-term field warming. Glob. Chang. Biol. 23, 4765–4776 (2017).
Chen, J. et al. Differential responses of carbon-degrading enzyme activities to warming: Implications for soil respiration. Glob. Chang. Biol. 24, 4816–4826 (2018).
Anthony, M. A., Crowther, T. W., Maynard, D. S., van den Hoogen, J. & Averill, C. Distinct assembly processes and microbial communities constrain soil organic carbon formation. One Earth 2, 349–360 (2020).
Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).
Cotrufo, M. F., Ranalli, M. G., Haddix, M. L., Six, J. & Lugato, E. Soil carbon storage informed by particulate and mineral-associated organic matter. Nat. Geosci. 12, 989–994 (2019).
van Gestel, N. et al. Predicting soil carbon loss with warming. Nature 554, E4–E5 (2018).
Hawkes, C. V., Waring, B. G., Rocca, J. D. & Kivlin, S. N. Historical climate controls soil respiration responses to current soil moisture. Proc. Natl Acad. Sci. USA 114, 6322–6327 (2017).
Ning, D. et al. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat. Commun. 11, 4717 (2020).
Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).
Tifafi, M., Guenet, B. & Hatté, C. Large differences in global and regional total soil carbon stock estimates based on SoilGrids, HWSD, and NCSCD: Intercomparison and evaluation based on field data from USA, England, Wales, and France. Glob. Biogeochem. Cycles 32, 42–56 (2018).
Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Ågren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).
We thank the reviewers for their careful reading of our manuscript and their insightful comments and suggestions. This article was conceived as a result of the Thematic Session on ‘Microbial Feedbacks to Climate Change’ presented at the British Ecological Society Annual Meeting 2018 held in Birmingham (UK). P.G.-P. is supported by a Ramón y Cajal grant from the Spanish Ministry of Science and Innovation (RYC2018-024766-I).
The authors declare no competing interests.
Peer review information
Nature Reviews Earth & Environment thanks Ben Bond-Lamberty, who co-reviewed with Jinshi Jian; Jizhong Zhou and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The CHELSA database: https://chelsa-climate.org/
The SoilGrids database: https://soilgrids.org/
The SRDB: https://github.com/bpbond/srdb
About this article
Cite this article
García-Palacios, P., Crowther, T.W., Dacal, M. et al. Evidence for large microbial-mediated losses of soil carbon under anthropogenic warming. Nat Rev Earth Environ 2, 507–517 (2021). https://doi.org/10.1038/s43017-021-00178-4
Nature Communications (2022)
Unexpected microbial metabolic responses to elevated temperatures and nitrogen addition in subarctic soils under different land uses
Nature Reviews Microbiology (2022)