Abstract

Soil microorganisms control carbon losses from soils to the atmosphere1,2,3, yet their responses to climate warming are often short-lived and unpredictable4,5,6,7. Two mechanisms, microbial acclimation and substrate depletion, have been proposed to explain temporary warming effects on soil microbial activity8,9,10. However, empirical support for either mechanism is unconvincing. Here we used geothermal temperature gradients (>50 years of field warming)11 and a short-term experiment to show that microbial activity (gross rates of growth, turnover, respiration and carbon uptake) is intrinsically temperature sensitive and does not acclimate to warming (+6 °C) over weeks or decades. Permanently accelerated microbial activity caused carbon loss from soil. However, soil carbon loss was temporary because substrate depletion reduced microbial biomass and constrained the influence of microbes over the ecosystem. A microbial biogeochemical model12,13,14 showed that these observations are reproducible through a modest, but permanent, acceleration in microbial physiology. These findings reveal a mechanism by which intrinsic microbial temperature sensitivity and substrate depletion together dictate warming effects on soil carbon loss via their control over microbial biomass. We thus provide a framework for interpreting the links between temperature, microbial activity and soil carbon loss on timescales relevant to Earth’s climate system.

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Change history

  • 08 October 2018

    In the version of this Letter originally published, the name of the institute in affiliation 3 was incorrect; it read “Institute of Applied Systems Analysis” but should have read “International Institute for Applied Systems Analysis”. This has now been corrected.

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Acknowledgements

The authors thank K. Gavazov, M. Wagner and members of the Division of Terrestrial Ecosystem Research, University of Vienna, for discussions and comments on the manuscript. T.W.N.W. was funded by a JPI Climate Project (COUP-Austria; BMWFW-6.020/0008) awarded to A.R. The study was also supported by a European Research Council Synergy Grant (IMBALANCE-P; ERC-2013-SyG 610028) awarded to I.A.J and J. Peñuelas. F.S. was funded by a European Research Council Starting Grant (DormantMicrobes; 636928) awarded to D.W. C.W.H. was supported by a European Research Council Advanced Grant (NITRICARE; 294343) awarded to M. Wagner. B.D.S. was supported by the Icelandic Research Council (ForHot-Forest; 163272-051) and the ClimMani COST Action (ES1308).

Author information

Affiliations

  1. Department of Microbiology & Ecosystem Science, Division of Terrestrial Ecosystem Research, University of Vienna, Vienna, Austria

    • Tom W. N. Walker
    • , Christina Kaiser
    •  & Andreas Richter
  2. Department of Ecology & Evolution, Université de Lausanne, Lausanne, Switzerland

    • Tom W. N. Walker
  3. International Institute for Applied Systems Analysis, Laxenburg, Austria

    • Christina Kaiser
    •  & Andreas Richter
  4. Department of Microbiology & Ecosystem Science, Division of Microbial Ecology, University of Vienna, Vienna, Austria

    • Florian Strasser
    • , Craig W. Herbold
    •  & Dagmar Woebken
  5. Department of Biology, University of Antwerp, Antwerp, Belgium

    • Niki I. W. Leblans
    •  & Ivan A. Janssens
  6. Agricultural University of Iceland, Hvanneyri, Borgarnes, Iceland

    • Niki I. W. Leblans
    •  & Bjarni D. Sigurdsson

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Contributions

A.R. and T.W.N.W. conceived the study. N.I.W.L., B.D.S. and I.A.J. established the field sites. T.W.N.W. and A.R. carried out the fieldwork. T.W.N.W. performed the experiments, measurements and DNA extractions, and C.K. carried out the modelling. F.S. and C.W.H. undertook the metagenomic investigations, with supervision from D.W. T.W.N.W. analysed the data and wrote the manuscript in close collaboration with A.R. and C.K. and with input from all co-authors.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Tom W. N. Walker or Andreas Richter.

Supplementary information

  1. Supplementary Information

    Supplementary figures 1–7, Supplementary tables 1–4, Supplementary references

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DOI

https://doi.org/10.1038/s41558-018-0259-x

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