Skip to main content

Thank you for visiting 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.

Microbial mediation of carbon-cycle feedbacks to climate warming


Understanding the mechanisms of biospheric feedbacks to climate change is critical to project future climate warming1,2,3. Although microorganisms catalyse most biosphere processes related to fluxes of greenhouse gases, little is known about the microbial role in regulating future climate change4. Integrated metagenomic and functional analyses of a long-term warming experiment in a grassland ecosystem showed that microorganisms play crucial roles in regulating soil carbon dynamics through three primary feedback mechanisms: shifting microbial community composition, which most likely led to the reduced temperature sensitivity of heterotrophic soil respiration; differentially stimulating genes for degrading labile but not recalcitrant carbon so as to maintain long-term soil carbon stability and storage; and enhancing nutrient-cycling processes to promote plant nutrient-use efficiency and hence plant growth. Elucidating microbially mediated feedbacks is fundamental to understanding ecosystem responses to climate warming and provides a mechanistic basis for carbon–climate modelling.

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

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: Effects of warming on a series of plant and soil variables.
Figure 2: Impacts of warming on N cycling.
Figure 3: The normalized average signal intensity of detected C-degradation genes under warming and the control.


  1. Heimann, M. & Reichstein, M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008).

    Article  CAS  Google Scholar 

  2. Walther, G. R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    Article  CAS  Google Scholar 

  3. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    Article  CAS  Google Scholar 

  4. Bardgett, R. D., Freeman, C. & Ostle, N. J. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2, 805–814 (2008).

    Article  CAS  Google Scholar 

  5. IPCC Global Climate Projections (Cambridge Univ. Press), (2007).

  6. Luo, Y. Q. Terrestrial carbon-cycle feedback to climate warming. Annu. Rev. Ecol. Evol. Syst. 38, 683–712 (2007).

    Article  Google Scholar 

  7. Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).

    Article  CAS  Google Scholar 

  8. Friedlingstein, P. et al. Climate-carbon cycle feedback analysis: Results from the (CMIP)-M-4 model intercomparison. J. Clim. 19, 3337–3353 (2006).

    Article  Google Scholar 

  9. Luo, Y. Q., Sherry, R., Zhou, X. H. & Wan, S. Q. Terrestrial carbon-cycle feedback to climate warming: Experimental evidence on plant regulation and impacts of biofuel feedstock harvest. GCB Bioenergy 1, 62–74 (2009).

    Article  CAS  Google Scholar 

  10. Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nature Geosci. 3, 336–340 (2010).

    Article  CAS  Google Scholar 

  11. Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008).

    Article  CAS  Google Scholar 

  12. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).

    Article  CAS  Google Scholar 

  13. He, Z. et al. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. ISME J. 4, 1167–1179 (2010).

    Article  CAS  Google Scholar 

  14. He, Z. et al. GeoChip: A comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 1, 67–77 (2007).

    Article  CAS  Google Scholar 

  15. He, Z. et al. Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2 . Ecol. Lett. 13, 564–575 (2010).

    Article  Google Scholar 

  16. Zhou, J. Z, Kang, S., Schadt, C. W. & Garten, C. T. Spatial scaling of functional gene diversity across various microbial taxa. Proc. Natl Acad. Sci. USA 105, 7768–7773 (2008).

    Article  CAS  Google Scholar 

  17. 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  CAS  Google Scholar 

  18. Reich, P. B. et al. Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410, 809–812 (2001).

    Article  CAS  Google Scholar 

  19. Zhou, X., Wan, S. Q. & Luo, Y. Q. Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Glob. Change Biol. 13, 761–775 (2007).

    Google Scholar 

  20. 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 

  21. Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001).

    Article  CAS  Google Scholar 

  22. 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. Change Biol. 13, 1761–1770 (2007).

    Article  Google Scholar 

  23. Parton, W. J., Schimel, D. S., Cole, C. V. & Ojima, D. S. Analysis of factors controlling soil organic-matter levels in great-plains grasslands. Soil Sci. Soc. Am. J. 51, 1173–1179 (1987).

    Article  CAS  Google Scholar 

  24. Heim, A. & Schmidt, M. W. I. Lignin turnover in arable soil and grassland analysed with two different labelling approaches. Eur. J. Soil Sci. 58, 599–608 (2007).

    Article  CAS  Google Scholar 

  25. Kephart, K. D. & Buxton, D. R. Forage quality responses of C3 and C4 perennial grasses to shade. Crop Sci. 33, 831–837 (1993).

    Article  CAS  Google Scholar 

  26. Kramer, M. G., Sollins, P., Sletten, R. S. & Swart, P. K. N isotope fractionation and measures of organic matter alteration during decomposition. Ecology 84, 2021–2025 (2003).

    Article  Google Scholar 

  27. Wan, S. Q., Hui, D. F., Wallace, L. & Luo, Y. Q. Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Glob. Biogeochem. Cycles 19, GB2014 (2005).

    Article  Google Scholar 

  28. An, Y. A. et al. Plant nitrogen concentration, use efficiency, and contents in a tallgrass prairie ecosystem under experimental warming. Glob. Change Biol. 11, 1733–1744 (2005).

    Article  Google Scholar 

  29. Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl Acad. Sci. USA 105, 11512–11519 (2008).

    Article  CAS  Google Scholar 

  30. Zhou, J. Z., Bruns, M. A. & Tiedje, J. M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322 (1996).

    CAS  Google Scholar 

Download references


This work is supported by the US Department of Energy, Biological Systems Research on the Role of Microbial Communities in Carbon Cycling Program (DE-SC0004601), and Oklahoma Bioenergy Center (OBC). The GeoChips and associated computational pipelines used in this study were supported by ENIGMA—Ecosystems and Networks Integrated with Genes and Molecular Assemblies through the Office of Science, Office of Biological and Environmental Research, the US Department of Energy under Contract No. DE-AC02-05CH11231 and by the US Department of Agriculture (Project 2007-35319-18305) through the NSF-USDA Microbial Observatories Program.

Author information

Authors and Affiliations



All authors contributed intellectual input and assistance to this study and manuscript preparation. The original concept and experimental strategy were developed by J.Z. and L.W. Sampling collections, DNA preparation, GeoChip and pyrosequencing analysis were carried out by Y.D., J.X. and L.W. K.X. carried out soil chemical analysis and various statistical analyses with Y.D., and S.F. carried out modelling analysis. S.D. carried out soil enzyme analysis. Z.H., Y.D. and J.D.V.N. assisted with GeoChip and sequencing analysis. J.Z. and Y.L. guided all data analysis and integration. J.Z. and K.X. wrote the paper with help from Y.L. and Z.H.

Corresponding author

Correspondence to Jizhong Zhou.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 909 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zhou, J., Xue, K., Xie, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nature Clim Change 2, 106–110 (2012).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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