Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Soil-carbon response to warming dependent on microbial physiology

Abstract

Most ecosystem models predict that climate warming will stimulate microbial decomposition of soil carbon, producing a positive feedback to rising global temperatures1,2. Although field experiments document an initial increase in the loss of CO2 from soils in response to warming, in line with these predictions, the carbon dioxide loss from soils tends to decline to control levels within a few years3,4,5. This attenuation response could result from changes in microbial physiological properties with increasing temperature, such as a decline in the fraction of assimilated carbon that is allocated to growth, termed carbon-use efficiency6. Here we explore these mechanisms using a microbial-enzyme model to simulate the responses of soil carbon to warming by 5 C. We find that declines in microbial biomass and degradative enzymes can explain the observed attenuation of soil-carbon emissions in response to warming. Specifically, reduced carbon-use efficiency limits the biomass of microbial decomposers and mitigates the loss of soil carbon. However, microbial adaptation or a change in microbial communities could lead to an upward adjustment of the efficiency of carbon use, counteracting the decline in microbial biomass and accelerating soil-carbon loss. We conclude that the soil-carbon response to climate warming depends on the efficiency of soil microbes in using carbon.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Diagram of soil C models.
Figure 2: Modelled soil CO2 and carbon-pool responses to 5 C warming in the enzyme-driven model.
Figure 3: Modelled soil CO2 and carbon-pool responses to 5 C warming in the conventional model.

References

  1. Friedlingstein, P. et al. Climate–carbon cycle feedback analysis: Results from the C4MIP model intercomparison. J. Clim. 19, 3337–3353 (2006).

    Article  Google Scholar 

  2. Lloyd, J. & Taylor, J. A. On the temperature dependence of soil respiration. Funct. Ecol. 8, 315–323 (1994).

    Article  Google Scholar 

  3. Luo, Y. Q., Wan, S. Q., Hui, D. F. & Wallace, L. L. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413, 622–625 (2001).

    Article  Google Scholar 

  4. Melillo, J. M. et al. Soil warming and carbon-cycle feedbacks to the climate system. Science 298, 2173–2176 (2002).

    Article  Google Scholar 

  5. Oechel, W. C. et al. Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406, 978–981 (2000).

    Article  Google Scholar 

  6. 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).

    Article  Google Scholar 

  7. Eliasson, P. E. et al. The response of heterotrophic CO2 flux to soil warming. Glob. Change Biol. 11, 167–181 (2005).

    Article  Google Scholar 

  8. Kirschbaum, M. U. F. Soil respiration under prolonged soil warming: Are rate reductions caused by acclimation or substrate loss? Glob. Change Biol. 10, 1870–1877 (2004).

    Article  Google Scholar 

  9. Knorr, W., Prentice, I. C., House, J. I. & Holland, E. A. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301 (2005).

    Article  Google Scholar 

  10. Schimel, J. P. & Weintraub, M. N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: A theoretical model. Soil Biol. Biochem. 35, 549–563 (2003).

    Article  Google Scholar 

  11. Fontaine, S. & Barot, S. Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol. Lett. 8, 1075–1087 (2005).

    Article  Google Scholar 

  12. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Article  Google Scholar 

  13. 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. Change Biol. 15, 2950–2957 (2009).

    Article  Google Scholar 

  14. Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).

    Article  Google Scholar 

  15. Saleska, S. R., Harte, J. N. & Torn, M. S. The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow. Glob. Change Biol. 5, 125–141 (1999).

    Article  Google Scholar 

  16. Waldrop, M. P., Balser, T. C. & Firestone, M. K. Linking microbial community composition to function in a tropical soil. Soil Biol. Biochem. 32, 1837–1846 (2000).

    Article  Google Scholar 

  17. López-Urrutia, Á. & Morán, X. A. G. Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88, 817–822 (2007).

    Article  Google Scholar 

  18. Rinnan, R., Michelsen, A., Bååth, E. & Jonasson, S. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob. Change Biol. 13, 28–39 (2007).

    Article  Google Scholar 

  19. Allison, S. D. & Treseder, K. K. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob. Change Biol. 14, 2898–2909 (2008).

    Article  Google Scholar 

  20. Schuur, E. A. G. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).

    Article  Google Scholar 

  21. Jonasson, S., Castro, J. & Michelson, A. Litter, warming and plants affect respiration and allocation of soil microbial and plant C, N and P in arctic mesocosms. Soil Biol. Biochem. 36, 1129–1139 (2004).

    Article  Google Scholar 

  22. Hochachka, P. W. & Somero, G. N. Biochemical Adaptation: Mechanism and Process in Physiological Evolution (Oxford Univ. Press, 2002).

    Google Scholar 

  23. Raich, J. W., Russell, A. E., Kitayama, K., Parton, W. J. & Vitousek, P. M. Temperature influences carbon accumulation in moist tropical forests. Ecology 87, 76–87 (2006).

    Article  Google Scholar 

  24. 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).

    Article  Google Scholar 

  25. Mack, M. C., Schuur, E. A. G., Bret-Harte, M. S., Shaver, G. R. & Chapin, F. S. III. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 433, 440–443 (2004).

    Article  Google Scholar 

  26. Liu, W., Zhang, Z. & Wan, S. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob. Change Biol. 15, 184–195 (2009).

    Article  Google Scholar 

  27. Bonan, G. Carbon cycle: Fertilizing change. Nature Geosci. 1, 645–646 (2008).

    Article  Google Scholar 

  28. Bosatta, E. & Ågren, G. I. Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 31, 1889–1891 (1999).

    Article  Google Scholar 

  29. Six, J., Frey, S. D., Thiet, R. K. & Batten, K. M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 70, 555–569 (2006).

    Article  Google Scholar 

  30. Trasar-Cepeda, C., Gil-Sotres, F. & Leirós, M. C. Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biol. Biochem. 39, 311–319 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

R. Conant, W. Parton and G. Ågren commented on the manuscript. M.D.W. and M.A.B. were supported by the US Department of Energy’s Office of Science (BER), S.D.A. by NSF Advancing Theory in Biology, and M.D.W. by DOE’s Northeastern Regional Center of the National Institute for Climatic Change Research, the USDA CSREES and NSF Ecosystems. The work is also a product of the NSF-supported Research Coordination Network on Enzymes in the Environment.

Author information

Authors and Affiliations

Authors

Contributions

M.A.B. and M.D.W. conceived the project, and S.D.A. built the model. S.D.A. and M.A.B. conducted model runs. All authors contributed to writing the paper.

Corresponding author

Correspondence to Steven D. Allison.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 519 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Allison, S., Wallenstein, M. & Bradford, M. Soil-carbon response to warming dependent on microbial physiology. Nature Geosci 3, 336–340 (2010). https://doi.org/10.1038/ngeo846

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo846

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing