Letter | Published:

Temperature sensitivity of soil respiration rates enhanced by microbial community response

Nature 513, 81–84 (04 September 2014) | Download Citation

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Abstract

Soils store about four times as much carbon as plant biomass1, and soil microbial respiration releases about 60 petagrams of carbon per year to the atmosphere as carbon dioxide2. Short-term experiments have shown that soil microbial respiration increases exponentially with temperature3. This information has been incorporated into soil carbon and Earth-system models, which suggest that warming-induced increases in carbon dioxide release from soils represent an important positive feedback loop that could influence twenty-first-century climate change4. The magnitude of this feedback remains uncertain, however, not least because the response of soil microbial communities to changing temperatures has the potential to either decrease5,6,7 or increase8,9 warming-induced carbon losses substantially. Here we collect soils from different ecosystems along a climate gradient from the Arctic to the Amazon and investigate how microbial community-level responses control the temperature sensitivity of soil respiration. We find that the microbial community-level response more often enhances than reduces the mid- to long-term (90 days) temperature sensitivity of respiration. Furthermore, the strongest enhancing responses were observed in soils with high carbon-to-nitrogen ratios and in soils from cold climatic regions. After 90 days, microbial community responses increased the temperature sensitivity of respiration in high-latitude soils by a factor of 1.4 compared to the instantaneous temperature response. This suggests that the substantial carbon stores in Arctic and boreal soils could be more vulnerable to climate warming than currently predicted.

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Acknowledgements

We thank the staff of the Forestry Commission at Alice Holt Forest , T. Taylor from RSPB Aylesbeare Common Reserve, J. Harris from Cranfield University, C. Moscatelli and S. Marinari from Tuscia University, J. A. Carreira de la Fuente from the University of Jaén, R. Giesler from Umeå University and E. Cosio from The Pontifical Catholic University of Peru for help with site selection and soil sampling. We thank N. England for technical assistance with constructing the incubation system, J. Zaragoza Castells for help with soil sampling, A. Elliot for conducting the particle size analyses, J. Grapes for help with carbon and nitrogen analysis and S. Rouillard, H. Jones and T. Kurtén for assistance with graphics. This work was carried out with Natural Environment Research Council (NERC) funding (grant number NE/H022333/1). K.K. was supported by an Academy of Finland post-doctoral research grant while finalizing this manuscript. P.M. was supported by ARC FT110100457 and NERC NE/G018278/1, and B.K.S by the Grain Research and Development Corporation and ARC DP130104841.

Author information

    • Kristiina Karhu

    Present address: Department of Forest Sciences, University of Helsinki, 00014 Helsinki, Finland.

Affiliations

  1. Geography, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4RJ, UK

    • Kristiina Karhu
    •  & Iain P. Hartley

  2. Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, UK

    • Marc D. Auffret
    •  & James I. Prosser

  3. Rothamsted Research—North Wyke, Okehampton, Devon EX20 2SB, UK

    • Jennifer A. J. Dungait

  4. School of Agriculture, Food & Environment, The Royal Agricultural University, Cirencester, Gloucestershire GL7 6JS, UK

    • David W. Hopkins

  5. Hawkesbury Institute for the Environment, University of Western Sydney, Penrith 2751, New South Wales, Australia

    • Brajesh K. Singh

  6. School of Natural Sciences, Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK

    • Jens-Arne Subke

  7. School of Life Sciences, Heriot–Watt University, Edinburgh EH14 4AS, UK

    • Philip A. Wookey

  8. Department of Ecology, Swedish University of Agricultural Sciences (SLU), 750 07 Uppsala, Sweden

    • Göran I. Ågren

  9. Laboratory of Functional Ecology and Global Change, Forest Sciences Centre of Catalonia (CTFC), 25280 Solsona, Spain

    • Maria-Teresa Sebastià
    •  & Fabrice Gouriveau

  10. Department of Horticulture, Botany and Landscaping, School of Agrifood and Forestry Science and Engineering, University of Lleida, 25198 Lleida, Spain

    • Maria-Teresa Sebastià

  11. Department of Crop Production Ecology, Swedish University of Agricultural Sciences (SLU), 750 07 Uppsala, Sweden

    • Göran Bergkvist

  12. School of Geosciences, University of Edinburgh, Edinburgh EH8 9XP, UK

    • Patrick Meir
    •  & Andrew T. Nottingham

  13. Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, Australia

    • Patrick Meir

  14. Seccion Quimica, Pontificia Universidad Catolica del Peru, Lima 32, Peru

    • Norma Salinas

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Contributions

K.K. conducted the CO2 measurements and statistical analyses. K.K. and M.D.A. conducted the chloroform-fumigation extraction and qPCR analyses, respectively, and led the data analysis and interpretation. I.P.H. (lead investigator), P.A.W., D.W.H., B.K.S. and J.I.P. designed the study. G.I.Å. and K.K. were responsible for the modelling presented in the methods. K.K., I.P.H., J.A.J.D., D.W.H., J.-A.S., P.A.W., M.-T.S., F.G., G.B., P.M., A.T.N. and N.S. were involved in planning site selection and soil sampling. All authors were involved in interpreting the results and contributed to writing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Kristiina Karhu.

Extended data

Extended data figures

  1. 1.

    The results of the Q model, presenting the patterns that would be observed if there were no compensatory or enhancing microbial community responses.

  2. 2.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 1A, 1C, 1D and 1G, including the 84-day pre-incubation period.

  3. 3.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 1H, 2C, 2D and 2G, including the 84-day pre-incubation period.

  4. 4.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 2H, 3A, 3C and 3D, including the 84-day pre-incubation period.

  5. 5.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 3G, 3H, 4A and 4C, including the 84-day pre-incubation period.

  6. 6.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 4D, 4G, 4H and 5E_1, including the 84-day pre-incubation period.

  7. 7.

    Respiration rates of all treatments (control, cooled and re-warmed) for the individual soils 5E_2 and 5E_3, including the 84-day pre-incubation period.

  8. 8.

    The mean ± 95% confidence intervals of mass-specific RRMT values, calculated per CFE biomass (a) and per qPCR biomass (b).

Extended data tables

  1. 1.

    Sampling site and soil characteristics

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and Supplementary Tables 1-3.

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DOI

https://doi.org/10.1038/nature13604

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