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Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation

Abstract

Climate warming may stimulate microbial metabolism of soil carbon, causing a carbon-cycle–climate feedback whereby carbon is redistributed from the soil to atmospheric CO2. The magnitude of this feedback is uncertain, in part because warming-induced shifts in microbial physiology and/or community composition could retard or accelerate soil carbon losses. Here, we measure microbial respiration rates for soils collected from 22 sites in each of 3 years, at locations spanning boreal to tropical climates. Respiration was measured in the laboratory with standard temperatures, moisture and excess carbon substrate, to allow physiological and community effects to be detected independent of the influence of these abiotic controls. Patterns in respiration for soils collected across the climate gradient are consistent with evolutionary theory on physiological responses that compensate for positive effects of temperature on metabolism. Respiration rates per unit microbial biomass were as much as 2.6 times higher for soils sampled from sites with a mean annual temperature of −2.0 versus 21.7 °C. Subsequent 100-d incubations suggested differences in the plasticity of the thermal response among microbial communities, with communities sampled from sites with higher mean annual temperature having a more plastic response. Our findings are consistent with adaptive metabolic responses to contrasting thermal regimes that are also observed in plants and animals. These results may help build confidence in soil-carbon–climate feedback projections by improving understanding of microbial processes represented in biogeochemical models.

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Fig. 1: Competing assumptions for adaptive responses of soil microbial respiration to changes in thermal climate.
Fig. 2: Estimated effects of spatial variation in thermal climate (observational gradient) on soil microbial respiration rates.
Fig. 3: Estimated effects of experimental variation in thermal climate (incubator gradient)—with substrate supply—on soil microbial respiration rates.
Fig. 4: Estimated effects of experimental variation in thermal climate (incubator gradient)—without substrate supply—on soil microbial respiration rates.

Data availability

Data in the support of these findings and the R code for the statistical models are available via the Dryad Digital Repository (https://doi.org/10.5061/dryad.s87008d).

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Acknowledgements

Research was supported by the US National Science Foundation with grants to M.A.B., R.L.M. and N.F. (DEB-1457614, -1021098, -1021222 and -1021112). This work was made possible by the generosity of researchers at the 11 locations who collected and packaged soils—in particular, A. Keiser, I. Halm, S. Bailey, M. Schulze, S. VanderWulp, P. O’Neal, T. Van Slyke, K. Chowanski, J. Love, A. Barker Plotkin, S. Cantrell and C. Giardina. Thanks also to J. Nelson for the PLFA analyses, and the Bradford laboratory group and M. Dacal for comments on an earlier version of the manuscript.

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M.A.B., R.L.M. and N.F. co-designed the study and wrote the application for the grant that funded the work. M.A.B., R.L.M., E.E.O. and T.W.C. collected the data and performed the laboratory work. S.A.W. and M.A.B. carried out the statistical analyses. All authors contributed to interpreting the data and writing the paper.

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Correspondence to Mark A. Bradford.

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Bradford, M.A., McCulley, R.L., Crowther, T.W. et al. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nat Ecol Evol 3, 223–231 (2019). https://doi.org/10.1038/s41559-018-0771-4

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