OpenLB
Open Library of Bioscience
Advanced Search
Nature ecology & evolution
02, 2023;7 (2): 205-213.

Temperature fluctuation promotes the thermal adaptation of soil microbial respiration.

Yan Zhang, Jin-Tao Li, Xiao Xu, Hong-Yang Chen, Ting Zhu, Jian-Jun Xu, Xiao-Ni Xu, Jin-Quan Li, Chao Liang, Bo Li, Chang-Ming Fang, Ming Nie
Author Information
  1. Yan Zhang: 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. ORCID
  2. Jin-Tao Li: 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.
  3. Xiao Xu: 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.
  4. Hong-Yang Chen: 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.
  5. Ting Zhu: 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. ORCID
  6. Jian-Jun Xu: 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.
  7. Xiao-Ni Xu: 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.
  8. Jin-Quan Li: 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.
  9. Chao Liang: Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China. ORCID
  10. Bo Li: 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. ORCID
  11. Chang-Ming Fang: 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.
  12. Ming Nie: 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. mnie@fudan.edu.cn. ORCID
PMID: 36635341 DOI: 10.1038/s41559-022-01944-3

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 CO concentrations than predicted.

References

Auffret, M. D. et al. The role of microbial community composition in controlling soil respiration responses to temperature. PLoS ONE 11, e0165448 (2016). [DOI: 10.1371/journal.pone.0165448]
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). [DOI: 10.1029/2020GB006918]
Davidson, E. A., Janssens, I. A. & Luo, Y. On the variability of respiration in terrestrial ecosystems: moving beyond Q. Glob. Change Biol. 12, 154–164 (2006). [DOI: 10.1111/j.1365-2486.2005.01065.x]
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). [DOI: 10.1002/2015JG003217]
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). [DOI: 10.1016/j.agrformet.2018.01.026]
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). [DOI: 10.1088/1748-9326/8/3/034034]
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). [DOI: 10.1111/j.1365-2486.2011.02546.x]
Oechel, W. C. et al. Acclimation of ecosystem CO exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406, 978–981 (2000). [DOI: 10.1038/35023137]
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). [DOI: 10.1111/gcb.15053]
Nie, M. et al. Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecol. Lett. 16, 234–241 (2013). [DOI: 10.1111/ele.12034]
Ji, F., Wu, Z., Huang, J. & Chassignet, E. P. Evolution of land surface air temperature trend. Nat. Clim. Change 4, 462–466 (2014). [DOI: 10.1038/nclimate2223]
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). [DOI: 10.1038/nature12310]
Hansen, J., Sato, M. & Ruedy, R. Perception of climate change. Proc. Natl Acad. Sci. USA 109, E2415–E2423 (2012). [DOI: 10.1073/pnas.1205276109]
Byrne, M. P. Amplified warming of extreme temperatures over tropical land. Nat. Geosci. 14, 837–841 (2021). [DOI: 10.1038/s41561-021-00828-8]
IPCC Climate Change 2021: The Physical Science Basis (eds Masson-Delmotte, V. et al.) (Cambridge Univ. Press, 2021).
Chan, W. P. et al. Seasonal and daily climate variation have opposite effects on species elevational range size. Science 351, 1437–1439 (2016). [DOI: 10.1126/science.aab4119]
Biederbeck, V. O. & Campbell, C. A. Soil microbial activity as influenced by temperature trends and fluctuations. Can. J. Soil Sci. 53, 363–375 (1973). [DOI: 10.4141/cjss73-053]
Karhu, K. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014). [DOI: 10.1038/nature13604]
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). [DOI: 10.1038/s41467-020-19549-4]
Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010). [DOI: 10.1038/ngeo846]
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). [DOI: 10.1111/ele.13379]
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). [DOI: 10.1007/s10533-021-00885-6]
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). [DOI: 10.1111/gcb.15878]
Feng, J. et al. Soil microbial trait-based strategies drive metabolic efficiency along an altitude gradient. ISME Commun. 1, 71 (2021). [DOI: 10.1038/s43705-021-00076-2]
Li, J. et al. Key microorganisms mediate soil carbon-climate feedbacks in forest ecosystems. Sci. Bull. 66, 2036–2044 (2021). [DOI: 10.1016/j.scib.2021.03.008]
Trivedi, P. et al. Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships. ISME J. 10, 2593–2604 (2016). [DOI: 10.1038/ismej.2016.65]
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). [DOI: 10.1016/j.soilbio.2010.12.021]
Bradford, M. A. et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11, 1316–1327 (2008). [DOI: 10.1111/j.1461-0248.2008.01251.x]
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). [DOI: 10.1111/j.1461-0248.2008.01223.x]
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). [DOI: 10.1038/s41559-018-0771-4]
Tian, W. et al. Thermal adaptation occurs in the respiration and growth of widely distributed bacteria. Glob. Change Biol. 28, 2820–2829 (2022). [DOI: 10.1111/gcb.16102]
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). [DOI: 10.1111/j.1365-2486.2009.02040.x]
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). [DOI: 10.1038/s41558-018-0259-x]
Chen, H. et al. Microbial respiratory thermal adaptation is regulated by r-/K-strategy dominance. Ecol. Lett. 25, 2489–2499 (2022). [DOI: 10.1111/ele.14106]
Wang, C. et al. The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization. ISME J. 15, 2738–2747 (2021). [DOI: 10.1038/s41396-021-00959-1]
Ramadhin, C., Yi, C. & Hendrey, G. Temperature variance portends and indicates the extent of abrupt climate shifts. IOP SciNotes 2, 014002 (2021). [DOI: 10.1088/2633-1357/abda14]
Sun, Y. Q. & Ge, Y. Temporal changes in the function of bacterial assemblages associated with decomposing earthworms. Front. Microbiol. 12, 682224 (2021). [DOI: 10.3389/fmicb.2021.682224]
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). [DOI: 10.1029/2019JG005095]
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). [DOI: 10.1038/ismej.2017.178]
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). [DOI: 10.1111/gcb.15553]
Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013). [DOI: 10.1126/science.1231923]
Qiao, N. et al. Labile carbon retention compensates for CO released by priming in forest soils. Glob. Change Biol. 20, 1943–1954 (2014). [DOI: 10.1111/gcb.12458]
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). [DOI: 10.1111/gcb.15819]
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). [DOI: 10.1029/2002GB001971]
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). [DOI: 10.1111/j.1365-2486.2009.02132.x]
Xia, J. et al. Terrestrial carbon cycle affected by non-uniform climate warming. Nat. Geosci. 7, 173–180 (2014). [DOI: 10.1038/ngeo2093]
Balesdent, J. et al. Atmosphere–soil carbon transfer as a function of soil depth. Nature 559, 599–602 (2018). [DOI: 10.1038/s41586-018-0328-3]
Howard, D. M. & Howard, P. J. A. Relationships between CO evolution, moisture-content and temperature for a range of soil types. Soil Biol. Biochem. 25, 1537–1546 (1993). [DOI: 10.1016/0038-0717(93)90008-Y]
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). [DOI: 10.1007/s00374-007-0237-3]
Mau, R. L. et al. Linking soil bacterial biodiversity and soil carbon stability. ISME J. 9, 1477–1480 (2015). [DOI: 10.1038/ismej.2014.205]
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). [DOI: 10.1111/gcb.12036]
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). [DOI: 10.1111/gcb.12029]
Li, J. et al. Biogeographic variation in temperature sensitivity of decomposition in forest soils. Glob. Change Biol. 26, 1873–1885 (2020). [DOI: 10.1111/gcb.14838]
Min, K. et al. Temperature sensitivity of biomass-specific microbial exo-enzyme activities and CO efflux is resistant to change across short- and long-term timescales. Glob. Change Biol. 5, 1793–1807 (2019). [DOI: 10.1111/gcb.14605]
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). [DOI: 10.1038/s41559-018-0770-5]
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). [DOI: 10.1097/NPT.0000000000000275]
Anderson, T. H. & Domsch, K. H. Soil microbial biomass: the eco-physiological approach. Soil Biol. Biochem. 12, 2039–2043 (2010). [DOI: 10.1016/j.soilbio.2010.06.026]
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). [DOI: 10.1016/0038-0717(87)90051-4]
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). [DOI: 10.1093/bioinformatics/btu170]
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011). [DOI: 10.14806/ej.17.1.200]
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). [DOI: 10.1093/bioinformatics/btr381]
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013). [DOI: 10.1038/nmeth.2604]
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019). [DOI: 10.1038/s41587-019-0209-9]
Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016). [DOI: 10.1038/nmeth.3869]
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). [DOI: 10.1093/nar/gks1219]
Koljalg, U. et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. N. Phytol. 166, 1063–1068 (2005). [DOI: 10.1111/j.1469-8137.2005.01376.x]
German, D. P. et al. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 43, 1387–1397 (2011). [DOI: 10.1016/j.soilbio.2011.03.017]
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). [DOI: 10.1163/156853806777239922]
Moinet, G. Y. K. et al. Temperature sensitivity of decomposition decreases with increasing soil organic matter stability. Sci. Total Environ. 704, 135460 (2020). [DOI: 10.1016/j.scitotenv.2019.135460]
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). [DOI: 10.1016/j.soilbio.2017.10.031]
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003). [DOI: 10.1111/j.1654-1103.2003.tb02228.x]

MeSH Term

Soil Microbiology
Temperature
Soil
Respiration
Carbon

Chemicals

Soil
Carbon
Journal Article Research Support, Non-U.S. Gov't

Word Cloud

Similar Articles

Cited By