Abstract
Soils are the largest repository of organic carbon (C) in the terrestrial biosphere and represent an important source of carbon dioxide (CO2) to the atmosphere, releasing 60–75 Pg C annually through microbial decomposition of organic materials1,2. A primary control on soil CO2 flux is the efficiency with which the microbial community uses C. Despite its critical importance to soil–atmosphere CO2 exchange, relatively few studies have examined the factors controlling soil microbial efficiency. Here, we measured the temperature response of microbial efficiency in soils amended with substrates varying in lability. We also examined the temperature sensitivity of microbial efficiency in response to chronic soil warming in situ. We find that the efficiency with which soil microorganisms use organic matter is dependent on both temperature and substrate quality, with efficiency declining with increasing temperatures for more recalcitrant substrates. However, the utilization efficiency of a more recalcitrant substrate increased at higher temperatures in soils exposed to almost two decades of warming 5 °C above ambient. Our work suggests that climate warming could alter the decay dynamics of more stable organic matter compounds, thereby having a positive feedback to climate that is attenuated by a shift towards a more efficient microbial community in the longer term.
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References
Schlesinger, W. H. & Andrews, J. A. Soil respiration and the global carbon cycle. Biogeochem. 48, 7–20 (2000).
Schimel, D. S. Terrestrial ecosystems and the carbon cycle. Glob. Change Biol. 1, 77–91 (1995).
Heimann, M. & Reichstein, M. Terrestrial ecosystsem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008).
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).
Melillo, J. M. et al. Soil warming and carbon-cycle feedbacks to the climate system. Science 298, 2173–2176 (2002).
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).
Luo, Y. Q., Wan, S. Q., Hui, D. F. & Wallace, L. L. Acclimitization of soil respiration to warming in a tall grass prairie. Nature 413, 622–625 (2001).
Conant, R. T. et al. Temperature and soil carbon decomposition—Synthesis of current knowledge and a way forward. Glob. Change Biol. 17, 3392–3404 (2011).
Del Giorgio, P. A. & Cole, J. J. Bacterial growth efficiency in natural aquatic systems. Ann. Rev. Ecol. Syst. 29, 503–541 (1998).
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).
Six, J., Frey, S. D., Thiet, R. K. & Batten, K. M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Amer. J. 70, 555–569 (2006).
Apple, J. K., del Giorgio, P. A. & Kemp, W. M. Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aqua. Microb. Ecol. 43, 243–254 (2006).
Lopez-Urrutia, A. & Moran, X. A. G. Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88, 817–822 (2007).
Rivkin, R. B. & Legendre, L. Biogenic carbon cycling in the upper ocean: Effects of microbial respiration. Science 291, 2398–2400 (2001).
Wetterstedt, J. Å. M. & Ågren, G. I. Quality or decomposer efficiency—Which is most important in the temperature response of litter decomposition? A modeling study using the GLUE methodology. Biogeoscience 8, 477–487 (2011).
Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nature Geosci. 3, 336–340 (2010).
Steinweg, J. M. et al. Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biol. Biochem. 40, 2722–2728 (2008).
Devevre, O. C. & Horwath, W. R. Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol. Biochem. 32, 1773–1785 (2000).
Dijkstra, P. et al. Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biol. Biochem. 43, 2023–2031 (2011).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).
Frey, S. D., Drijber, R., Smith, H. & Melillo, J. M. Microbial biomass, functional capacity, and community composition after twelve years of soil warming. Soil Biol. Biochem. 40, 2904–2907 (2008).
Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nature Clim. Change 2, 106–110 (2012).
Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).
Kroer, N. Bacterial growth efficiency on natural dissolved organic matter. Limnol. Oceanogr. 38, 1282–1290 (1993).
Contosta, A. R., Frey, S. D. & Cooper, A. B. Seasonal dynamics of soil respiration and nitrogen mineralization in chronically warmed and fertilized soils. Ecosphere 2, 1–21 (2011).
Del Grosso, S. et al. Simulated effects of dryland cropping intensification on soil organic matter and greenhouse gas exchanges using the DAYCENT ecosystem model. Environ. Poll 116, S75–S83 (2002).
Brant, J. B., Sulzman, E. W. & Myrold, D. D. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol. Biochem. 38, 2219–2232 (2006).
Frey, S. D., Gupta, V. V. S. R., Elliott, E. T. & Paustian, K. Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biol. Biochem. 33, 1759–1768 (2001).
Acknowledgements
M. Knorr, B. Godbois, J. Herszage and R. Rousseau provided laboratory assistance with sample analysis. Stable isotope measurements were conducted at the Stable Isotope Facility at the University of California—Davis. This work, including maintenance of the long-term soil warming experiments, was supported by an NSF Faculty Early Career Development Award, the NSF Long-term Ecological Research (LTER) Program, a DOE National Institute for Climatic Change Research (NICCR) grant, and a Harvard Forest Bullard Fellowship to S.D.F. We would especially like to acknowledge the NSF LTER programme for providing intellectual and financial support of long-term ecological experiments without which this work would not have been possible.
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S.D.F. and J.S. conceived the project. S.D.F. collected the soil samples, conducted the soil incubations, and led the data analysis and manuscript preparation. J.S. supervised the stable isotope analysis and modelling exercise and assisted with data interpretation. J.L. conducted the model runs. J.M.M. designed and conducted the long-term (18 year) soil warming experiment, made the in situ measurements of net nitrogen mineralization, and assisted with data interpretation. All authors contributed to writing the final manuscript.
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Frey, S., Lee, J., Melillo, J. et al. The temperature response of soil microbial efficiency and its feedback to climate. Nature Clim Change 3, 395–398 (2013). https://doi.org/10.1038/nclimate1796
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DOI: https://doi.org/10.1038/nclimate1796
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