Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Temperature fluctuation promotes the thermal adaptation of soil microbial respiration

Nature Ecology & Evolution volume 7, pages 205–213 (2023)Cite this article

Subjects

Abstract

The magnitude of the feedback between soil microbial respiration and increased mean temperature may decrease (a process called thermal adaptation) or increase over time, and accurately representing this feedback in models improves predictions of soil carbon loss rates. However, climate change entails changes not only in mean temperature but also in temperature fluctuation, and how this fluctuation regulates the thermal response of microbial respiration has never been systematically evaluated. By analysing subtropical forest soils from a 2,000 km transect across China, we showed that although a positive relationship between soil microbial biomass-specific respiration and temperature was observed under increased constant incubation temperature, an increasing temperature fluctuation had a stronger negative effect. Our results further indicated that changes in bacterial community composition and reduced activities of carbon degradation enzymes promoted the effect of temperature fluctuation. This adaptive response of soil microbial respiration suggests that climate warming may have a lesser exacerbating effect on atmospheric CO2 concentrations than predicted.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The thermal regimes used in the two incubation experiments.
Fig. 2: Thermal treatment response of Rmass under three assay temperatures (5, 15 and 25 °C).
Fig. 3: Log response ratios of Rmass under three assay temperatures (5, 15 and 25 °C) for three incubation scenarios.
Fig. 4: Structural equation modelling of the effects of selected drivers on Rmass.

Similar content being viewed by others

Data availability

The sequence data generated in the present study have been deposited in the NCBI GenBank Short Read Archive under accession number PRJNA809849. All data supporting the findings of the statistical analyses are publicly available at https://doi.org/10.5281/zenodo.6153431.

Code availability

All the R code for our statistical analyses is publicly available at https://doi.org/10.5281/zenodo.6153431.

References

  1. Auffret, M. D. et al. The role of microbial community composition in controlling soil respiration responses to temperature. PLoS ONE 11, e0165448 (2016).

    Article  Google Scholar 

  2. Yao, Y. et al. A data-driven global soil heterotrophic respiration dataset and the drivers of its inter‐annual variability. Glob. Biogeochem. Cycle 35, e2020GB006918 (2021).

    Article  CAS  Google Scholar 

  3. Davidson, E. A., Janssens, I. A. & Luo, Y. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob. Change Biol. 12, 154–164 (2006).

    Article  Google Scholar 

  4. Wang, Q. et al. Soil microbial respiration rate and temperature sensitivity along a north–south forest transect in eastern China: patterns and influencing factors. J. Geophys. Res. Biogeosci. 121, 399–410 (2016).

    Article  Google Scholar 

  5. Sihi, D. et al. Merging a mechanistic enzymatic model of soil heterotrophic respiration into an ecosystem model in two AmeriFlux sites of northeastern USA. Agric. Meteorol. 252, 155–166 (2018).

    Article  Google Scholar 

  6. Shao, P., Zeng, X., Moore, D. J. P. & Zeng, X. Soil microbial respiration from observations and Earth system models. Environ. Res. Lett. 8, 034034 (2013).

    Article  CAS  Google Scholar 

  7. Davidson, E. A., Samanta, S., Caramori, S. S. & Savage, K. The dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob. Change Biol. 18, 371–384 (2012).

    Article  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. Alster, C. J., von Fischer, J. C., Allison, S. D. & Treseder, K. K. Embracing a new paradigm for temperature sensitivity of soil microbes. Glob. Change Biol. 26, 3221–3229 (2020).

    Article  Google Scholar 

  10. Nie, M. et al. Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecol. Lett. 16, 234–241 (2013).

    Article  Google Scholar 

  11. Ji, F., Wu, Z., Huang, J. & Chassignet, E. P. Evolution of land surface air temperature trend. Nat. Clim. Change 4, 462–466 (2014).

    Article  Google Scholar 

  12. Huntingford, C., Jones, P. D., Livina, V. N., Lenton, T. M. & Cox, P. M. No increase in global temperature variability despite changing regional patterns. Nature 500, 327–330 (2013).

    Article  CAS  Google Scholar 

  13. Hansen, J., Sato, M. & Ruedy, R. Perception of climate change. Proc. Natl Acad. Sci. USA 109, E2415–E2423 (2012).

    Article  CAS  Google Scholar 

  14. Byrne, M. P. Amplified warming of extreme temperatures over tropical land. Nat. Geosci. 14, 837–841 (2021).

    Article  CAS  Google Scholar 

  15. IPCC Climate Change 2021: The Physical Science Basis (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, 2021).

  16. Chan, W. P. et al. Seasonal and daily climate variation have opposite effects on species elevational range size. Science 351, 1437–1439 (2016).

    Article  CAS  Google Scholar 

  17. Biederbeck, V. O. & Campbell, C. A. Soil microbial activity as influenced by temperature trends and fluctuations. Can. J. Soil Sci. 53, 363–375 (1973).

    Article  Google Scholar 

  18. Karhu, K. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014).

    Article  CAS  Google Scholar 

  19. Chen, H., Zhu, T., Li, B., Fang, C. & Nie, M. The thermal response of soil microbial methanogenesis decreases in magnitude with changing temperature. Nat. Commun. 11, 5733 (2020).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Nottingham, A. T. et al. Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient. Ecol. Lett. 22, 1889–1899 (2019).

    Article  Google Scholar 

  22. Alster, C. J., Robinson, J. M., Arcus, V. L. & Schipper, L. A. Assessing thermal acclimation of soil microbial respiration using macromolecular rate theory. Biogeochemistry 158, 131–141 (2022).

    Article  CAS  Google Scholar 

  23. Moinet, G. Y. K. et al. Soil microbial sensitivity to temperature remains unchanged despite community compositional shifts along geothermal gradients. Glob. Change Biol. 27, 6217–6231 (2021).

    Article  Google Scholar 

  24. Feng, J. et al. Soil microbial trait-based strategies drive metabolic efficiency along an altitude gradient. ISME Commun. 1, 71 (2021).

    Article  Google Scholar 

  25. Li, J. et al. Key microorganisms mediate soil carbon-climate feedbacks in forest ecosystems. Sci. Bull. 66, 2036–2044 (2021).

    Article  CAS  Google Scholar 

  26. Trivedi, P. et al. Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships. ISME J. 10, 2593–2604 (2016).

    Article  CAS  Google Scholar 

  27. Zhu, B. & Cheng, W. Constant and diurnally-varying temperature regimes lead to different temperature sensitivities of soil organic carbon decomposition. Soil Biol. Biochem. 43, 866–869 (2011).

    Article  CAS  Google Scholar 

  28. Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008).

    Article  Google Scholar 

  29. 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 

  30. Bradford, M. A. et al. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nat. Ecol. Evol. 3, 223–231 (2019).

    Article  Google Scholar 

  31. Tian, W. et al. Thermal adaptation occurs in the respiration and growth of widely distributed bacteria. Glob. Change Biol. 28, 2820–2829 (2022).

    Article  CAS  Google Scholar 

  32. Bradford, M. A., Watts, B. W. & Davies, C. A. Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob. Change Biol. 16, 1576–1588 (2010).

    Article  Google Scholar 

  33. Walker, T. W. N. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Change 8, 885–889 (2018).

    Article  CAS  Google Scholar 

  34. Chen, H. et al. Microbial respiratory thermal adaptation is regulated by r-/K-strategy dominance. Ecol. Lett. 25, 2489–2499 (2022).

    Article  Google Scholar 

  35. Wang, C. et al. The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization. ISME J. 15, 2738–2747 (2021).

    Article  CAS  Google Scholar 

  36. Ramadhin, C., Yi, C. & Hendrey, G. Temperature variance portends and indicates the extent of abrupt climate shifts. IOP SciNotes 2, 014002 (2021).

    Article  Google Scholar 

  37. Sun, Y. Q. & Ge, Y. Temporal changes in the function of bacterial assemblages associated with decomposing earthworms. Front. Microbiol. 12, 682224 (2021).

    Article  Google Scholar 

  38. Shi, Z., Xu, J., Li, X., Li, R. & Li, Q. Links of extracellular enzyme activities, microbial metabolism, and community composition in the river-impacted coastal waters. J. Geophys. Res. Biogeosci. 124, 3507–3520 (2019).

    Article  Google Scholar 

  39. Razanamalala, K. et al. Soil microbial diversity drives the priming effect along climate gradients: a case study in Madagascar. ISME J. 12, 451–462 (2017).

    Article  Google Scholar 

  40. Xu, M. et al. High microbial diversity stabilizes the responses of soil organic carbon decomposition to warming in the subsoil on the Tibetan Plateau. Glob. Change Biol. 27, 2061–2075 (2021).

    Article  CAS  Google Scholar 

  41. Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).

    Article  CAS  Google Scholar 

  42. Qiao, N. et al. Labile carbon retention compensates for CO2 released by priming in forest soils. Glob. Change Biol. 20, 1943–1954 (2014).

    Article  Google Scholar 

  43. Ning, Q. et al. Carbon limitation overrides acidification in mediating soil microbial activity to nitrogen enrichment in a temperate grassland. Glob. Change Biol. 27, 5976–5988 (2021).

    Article  CAS  Google Scholar 

  44. Wan, S. & Luo, Y. Substrate regulation of soil respiration in a tallgrass prairie: results of a clipping and shading experiment. Glob. Biogeochem. Cycle 17, 1054 (2003).

    Article  Google Scholar 

  45. Gillabel, J., Cebrian-Lopez, B., Six, J. & Merckx, R. Experimental evidence for the attenuating effect of SOM protection on temperature sensitivity of SOM decomposition. Glob. Change Biol. 16, 2789–2798 (2010).

    Article  Google Scholar 

  46. Xia, J. et al. Terrestrial carbon cycle affected by non-uniform climate warming. Nat. Geosci. 7, 173–180 (2014).

    Article  CAS  Google Scholar 

  47. Balesdent, J. et al. Atmosphere–soil carbon transfer as a function of soil depth. Nature 559, 599–602 (2018).

    Article  CAS  Google Scholar 

  48. Howard, D. M. & Howard, P. J. A. Relationships between CO2 evolution, moisture-content and temperature for a range of soil types. Soil Biol. Biochem. 25, 1537–1546 (1993).

    Article  Google Scholar 

  49. Hoyle, F. C., Murphy, D. V. & Brookes, P. C. Microbial response to the addition of glucose in low-fertility soils. Biol. Fertil. Soils 44, 571–579 (2008).

    Article  CAS  Google Scholar 

  50. Mau, R. L. et al. Linking soil bacterial biodiversity and soil carbon stability. ISME J. 9, 1477–1480 (2015).

    Article  CAS  Google Scholar 

  51. 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 

  52. Billings, S. A. & Ballantyne, F. T. How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming. Glob. Change Biol. 19, 90–102 (2013).

    Article  Google Scholar 

  53. Li, J. et al. Biogeographic variation in temperature sensitivity of decomposition in forest soils. Glob. Change Biol. 26, 1873–1885 (2020).

    Article  Google Scholar 

  54. Min, K. et al. Temperature sensitivity of biomass-specific microbial exo-enzyme activities and CO2 efflux is resistant to change across short- and long-term timescales. Glob. Change Biol. 5, 1793–1807 (2019).

    Article  Google Scholar 

  55. Dacal, M., Bradford, M. A., Plaza, C., Maestre, F. T. & Garcia-Palacios, P. Soil microbial respiration adapts to ambient temperature in global drylands. Nat. Ecol. Evol. 3, 232–238 (2019).

    Article  Google Scholar 

  56. Field-Fote, E. E. Mediators and moderators, confounders and covariates: exploring the variables that illuminate or obscure the “active ingredients” in neurorehabilitation. J. Neurol. Phys. Ther. 43, 83–84 (2019).

    Article  Google Scholar 

  57. Anderson, T. H. & Domsch, K. H. Soil microbial biomass: the eco-physiological approach. Soil Biol. Biochem. 12, 2039–2043 (2010).

    Article  Google Scholar 

  58. Vance, E. D., Brookes, P. C. & Jenkinson, D. S. Microbial biomass measurements in forest soils—the use of the chloroform fumigation incubation method in strongly acid soils. Soil Biol. Biochem. 19, 697–702 (1987).

    Article  CAS  Google Scholar 

  59. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  Google Scholar 

  60. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).

    Article  Google Scholar 

  61. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).

    Article  CAS  Google Scholar 

  62. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).

    Article  CAS  Google Scholar 

  63. Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).

    Article  CAS  Google Scholar 

  64. Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    Article  CAS  Google Scholar 

  65. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).

    Article  CAS  Google Scholar 

  66. Koljalg, U. et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. N. Phytol. 166, 1063–1068 (2005).

    Article  CAS  Google Scholar 

  67. German, D. P. et al. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 43, 1387–1397 (2011).

    Article  CAS  Google Scholar 

  68. Mazerolle, M. Improving data analysis in herpetology: using Akaike’s information criterion (AIC) to assess the strength of biological hypotheses. Amphib. Reptil. 2, 169–180 (2006).

    Article  Google Scholar 

  69. Moinet, G. Y. K. et al. Temperature sensitivity of decomposition decreases with increasing soil organic matter stability. Sci. Total Environ. 704, 135460 (2020).

    Article  CAS  Google Scholar 

  70. Moinet, G. Y. K. et al. The temperature sensitivity of soil organic matter decomposition is constrained by microbial access to substrates. Soil Biol. Biochem. 116, 333–339 (2018).

    Article  CAS  Google Scholar 

  71. Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (grant nos 31930070, 92251305 and 91951112), the Program of Shanghai Academic/Technology Research Leader (grant no. 21XD1420700), the ‘Shuguang Program’ supported by the Shanghai Education Development Foundation and the Shanghai Municipal Education Commission (grant no. 21SG02), and the Shanghai Pilot Program for Basic Research—Fudan University 21TQ1400100 (grant no. 21TQ004).

Author information

Authors and Affiliations

  1. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, National Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Institute of Eco-Chongming, School of Life Sciences, Fudan University, Shanghai, China

    Yan Zhang, Jin-Tao Li, Xiao Xu, Hong-Yang Chen, Ting Zhu, Jian-Jun Xu, Xiao-Ni Xu, Jin-Quan Li, Bo Li, Chang-Ming Fang & Ming Nie

  2. Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming, China

    Xiao Xu & Bo Li

  3. Research Center for Northeast Asia Carbon Sink, Center for Ecological Research, Key Laboratory of Sustainable Forest Ecosystem Management—Ministry of Education, School of Forestry, Northeast Forestry University, Harbin, China

    Hong-Yang Chen

  4. Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China

    Chao Liang

Authors
  1. Yan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jin-Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong-Yang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ting Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jian-Jun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiao-Ni Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jin-Quan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chao Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chang-Ming Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ming Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.N. developed the original ideas presented in the manuscript. Y.Z. completed the experiments with assistance from M.N., J.-Q.L., J.-T.L., C.L., C.-M.F. and X.X. Y.Z. performed the overall analysis with assistance from X.-N.X., H.-Y.C., T.Z., J.-J.X., M.N. and B.L. Y.Z. and M.N. wrote the first draft, and all authors jointly revised the manuscript.

Corresponding author

Correspondence to Ming Nie.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Gabriel Moinet and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1–10 and Figs. 1–5.

Reporting Summary.

Peer Review File.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Li, JT., Xu, X. et al. Temperature fluctuation promotes the thermal adaptation of soil microbial respiration. Nat Ecol Evol 7, 205–213 (2023). https://doi.org/10.1038/s41559-022-01944-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01944-3

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene