Microbial temperature sensitivity and biomass change explain soil carbon loss with warming

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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Fig. 1: Soil microbial responses to long-term warming.
Fig. 2: Simulated responses to warming.
Fig. 3: Soil carbon cycle responses to climate warming.

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.

References

  1. 1.

    IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013) .

  2. 2.

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

    CAS  Article  Google Scholar 

  3. 3.

    Melillo, J. M. et al. Soil warming and carbon-cycle feedbacks to the climate system. Science 298, 2173–2176 (2002).

    CAS  Article  Google Scholar 

  4. 4.

    Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 2–7 (2016).

    Article  Google Scholar 

  5. 5.

    Luo, Y. Q., Wan, S. Q., Hui, D. F. & Wallace, L. L. Acclimatization of soil respiration to warming in a tall grass prairie. Ecol. Lett. 413, 622–625 (2001).

    CAS  Google Scholar 

  6. 6.

    Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Ecol. Lett. 104, 104–108 (2016).

    Google Scholar 

  7. 7.

    Melillo, J. M. et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105 (2017).

    CAS  Article  Google Scholar 

  8. 8.

    Hartley, I. P., Hopkins, D. W., Garnett, M. H., Sommerkorn, M. & Wookey, P. A. Soil microbial respiration in arctic soil does not acclimate to temperature. Ecol. Lett. 11, 1092–1100 (2008).

    Article  Google Scholar 

  9. 9.

    Crowther, T. W. & Bradford, M. A. Thermal acclimation in widespread heterotrophic soil microbes. Ecol. Lett. 16, 469–477 (2013).

    Article  Google Scholar 

  10. 10.

    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 

  11. 11.

    Sigurdsson, B. D. et al. Geothermal ecosystems as natural climate change experiments: the FORHOT research site in Iceland as a case study. Iceland Agricult. Sci. 29, 53–71 (2016).

    Article  Google Scholar 

  12. 12.

    Kaiser, C., Franklin, O., Dieckmann, U. & Richter, A. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol. Lett. 17, 680–690 (2014).

    Article  Google Scholar 

  13. 13.

    Kaiser, C., Franklin, O., Richter, A. & Dieckmann, U. Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils. Nat. Commun. 6, 8960 (2015).

    CAS  Article  Google Scholar 

  14. 14.

    Evans, S., Dieckmann, U., Franklin, O. & Kaiser, C. Synergistic effects of diffusion and microbial physiology reproduce the Birch effect in a micro-scale model. Soil Biol. Biochem. 93, 28–37 (2016).

    CAS  Article  Google Scholar 

  15. 15.

    Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3, 909–912 (2013).

    CAS  Article  Google Scholar 

  16. 16.

    Bradford, M. A. et al. Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Change 6, 751–758 (2016).

    Article  Google Scholar 

  17. 17.

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

    CAS  Article  Google Scholar 

  18. 18.

    Frey, S. D., Lee, J., Melillo, J. M. & Six, J. The temperature response of soil microbial efficiency and its feedback to climate. Nat. Clim. Change 3, 395–398 (2013).

    CAS  Article  Google Scholar 

  19. 19.

    Plante, A. F., Stone, M. M. & McGill, W. B. in Soil Microbiology, Ecology and Biochemistry (ed. Paul, E. A.) 245–272 (Elsevier, 2015).

    Google Scholar 

  20. 20.

    Bradford, M. A. Thermal adaptation of decomposer communities in warming soils. Front. Microbiol. 4, 333 (2013).

    Article  Google Scholar 

  21. 21.

    Yergeau, E. et al. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME J. 6, 692–702 (2011).

    Article  Google Scholar 

  22. 22.

    Tucker, C. L., Bell, J., Pendall, E. & Ogle, K. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob. Change Biol. 19, 252–263 (2013).

    Article  Google Scholar 

  23. 23.

    Spohn, M., Klaus, K., Wanek, W. & Richter, A. Microbial carbon use efficiency and biomass turnover times depending on soil depth—implications for carbon cycling. Soil Biol. Biochem. 96, 74–81 (2016).

    CAS  Article  Google Scholar 

  24. 24.

    Radujkovic, D. et al. Prolonged exposure does not increase soil microbial community response to warming along geothermal gradients. FEMS Microbiol. Ecol. 94, fix174 (2018).

    Article  Google Scholar 

  25. 25.

    Blagodatskaya, Е, Blagodatsky, S., Khomyakov, N., Myachina, O. & Kuzyakov, Y. Temperature sensitivity and enzymatic mechanisms of soil organic matter decomposition along an altitudinal gradient on Mount Kilimanjaro. Nat. Sci. Rep. 6, 22240 (2016).

    CAS  Article  Google Scholar 

  26. 26.

    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).

    CAS  Article  Google Scholar 

  27. 27.

    Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A. & Cleveland, C. C. Global patterns in belowground communities. Ecol. Lett. 12, 1238–1249 (2009).

    Article  Google Scholar 

  28. 28.

    Serna-Chavez, H. M., Fierer, N. & van Bodegom, P. M. Global drivers and patterns of microbial abundance in soil. Glob. Ecol. Biogeog. 22, 1162–1172 (2013).

    Article  Google Scholar 

  29. 29.

    Herbold, C. W. et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front. Microbiol. 6, 731 (2015).

    Article  Google Scholar 

  30. 30.

    Bengtsson-Palme, J. et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).

    Google Scholar 

  31. 31.

    Deshpande, V. et al. Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5 (2016).

    Article  Google Scholar 

  32. 32.

    Georgiou, K. et al. Microbial community-level regulation explains soil carbon responses to long-term litter manipulations. Nat. Commun. 8, 1223 (2017).

    Article  Google Scholar 

  33. 33.

    Carini, P. et al. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Ecol. Lett. 53, 680840 (2016).

    Google Scholar 

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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).

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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.

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

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The authors declare no competing interests.

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

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Walker, T.W.N., Kaiser, C., Strasser, F. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nature Clim Change 8, 885–889 (2018). https://doi.org/10.1038/s41558-018-0259-x

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