Abstract
Respiratory release of CO2 by microorganisms is one of the main components of the global carbon cycle. However, there are large uncertainties regarding the effects of climate warming on the respiration of microbial communities, owing to a lack of mechanistic, empirically tested theory that incorporates dynamic species interactions. We present a general mathematical model which predicts that thermal sensitivity of microbial community respiration increases as species interactions change from competition to facilitation (for example, commensalism, cooperation and mutualism). This is because facilitation disproportionately increases positive feedback between the thermal sensitivities of species-level metabolic and biomass accumulation rates at warmer temperatures. We experimentally validate our theoretical predictions in a community of eight bacterial taxa and show that a shift from competition to facilitation, after a month of co-adaptation, caused a 60% increase in the thermal sensitivity of respiration relative to de novo assembled communities that had not co-adapted. We propose that rapid changes in species interactions can substantially change the temperature dependence of microbial community respiration, which should be accounted for in future climate–carbon cycle models.
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Data availability
All data to reproduce our results are at https://doi.org/10.5281/zenodo.7105128.
Code availability
All code to reproduce our results are at https://doi.org/10.5281/zenodo.7105128.
References
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).
Lopez-Urrutia, A., San Martin, E., Harris, R. P. & Irigoien, X. Scaling the metabolic balance of the oceans. Proc. Natl Acad. Sci. USA 103, 8739–8744 (2006).
Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476 (2012).
Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).
Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).
Rivkin, R. B. & Legendre, L. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291, 2398–2400 (2001).
Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).
Smith, T. P. et al. Community-level respiration of prokaryotic microbes may rise with global warming. Nat. Commun. 10, 5124 (2019).
Antwis, R. E. et al. Fifty important research questions in microbial ecology. FEMS Microbiol. Ecol. 93, fix044 (2017).
Bardgett, R. D., Freeman, C. & Ostle, N. J. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2, 805–814 (2008).
Enquist, B. J. et al. Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theories. Adv. Ecol. Res. 52, 249–318 (2015).
Allen, A. P., Gillooly, J. F. & Brown, J. H. Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19, 202–213 (2005).
Schramski, J. R., Dell, A. I., Grady, J. M., Sibly, R. M. & Brown, J. H. Metabolic theory predicts whole-ecosystem properties. Proc. Natl Acad. Sci. USA 112, 2617–2622 (2015).
Alster, C. J., Koyama, A., Johnson, N. G., Wallenstein, M. D. & von Fischer, J. C. Temperature sensitivity of soil microbial communities: an application of macromolecular rate theory to microbial respiration. J. Geophys. Res. Biogeosci. 121, 1420–1433 (2016).
Yvon-Durocher, G. et al. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol. 13, e1002324 (2015).
Garzke, J., Connor, S. J., Sommer, U. & O’Connor, M. I. Trophic interactions modify the temperature dependence of community biomass and ecosystem function. PLoS Biol. 17, e2006806 (2019).
Foster, K. R. & Bell, T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22, 1845–1850 (2012).
Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).
Machado, D. et al. Polarization of microbial communities between competitive and cooperative metabolism. Nat. Ecol. Evol. 5, 195–203 (2021).
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).
Garcia-Martin, E. E., McNeill, S., Serret, P. & Leakey, R. J. G. Plankton metabolism and bacterial growth efficiency in offshore waters along a latitudinal transect between the UK and Svalbard. Deep Sea Res. I 92, 141–151 (2014).
Davidson, E. A., Richardson, A. D., Savage, K. E. & Hollinger, D. Y. A distinct seasonal pattern of the ratio of soil respiration to total ecosystem respiration in a spruce-dominated forest. Glob. Change Biol. 12, 230–239 (2006).
Dutkiewicz, S., Follows, M. J. & Bragg, J. G. Modeling the coupling of ocean ecology and biogeochemistry. Glob. Biogeochem. Cycles 23, GB4017 (2009).
Follows, M. J., Dutkiewicz, S., Ward, B. & Follett, C. in Microbial Ecology of the Oceans 3rd edn (eds Gasol, J. & Kirchman, D.) Ch. 12 (John Wiley, 2018).
Letten, A. D. & Stouffer, D. B. The mechanistic basis for higher-order interactions and non-additivity in competitive communities. Ecol. Lett. 22, 423–436 (2019).
Grilli, J., Barabás, G., Michalska-Smith, M. J. & Allesina, S. Higher-order interactions stabilize dynamics in competitive network models. Nature 548, 210–213 (2017).
Maynard, D. S., Crowther, T. W. & Bradford, M. A. Competitive network determines the direction of the diversity–function relationship. Proc. Natl Acad. Sci. USA 114, 11464–11469 (2017).
Fiegna, F., Moreno-Letelier, A., Bell, T. & Barraclough, T. G. Evolution of species interactions determines microbial community productivity in new environments. ISME J. 9, 1235–1245 (2015).
Lawrence, D. et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 10, e1001330 (2012).
Harcombe, W. R., Chacón, J. M., Adamowicz, E. M., Chubiz, L. M. & Marx, C. J. Evolution of bidirectional costly mutualism from byproduct consumption. Proc. Natl Acad. Sci. USA 115, 12000–12004 (2018).
Goldford, J. E. et al. Emergent simplicity in microbial community assembly. Science 361, 469–474 (2018).
Yvon-Durocher, G. et al. Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507, 488–491 (2014).
Fox, J. W. & Harpole, W. S. Revealing how species loss affects ecosystem function: the trait-based price equation partition. Ecology 89, 269–279 (2008).
Kontopoulos, D., Smith, T. P., Barraclough, T. G. & Pawar, S. Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate. PLoS Biol. 18, e3000894 (2020).
Wilson, W. G. & Lundberg, P. Biodiversity and the Lotka–Volterra theory of species interactions: open systems and the distribution of logarithmic densities. Proc. R. Soc. Lond. B 271, 1977–1984 (2004).
Rossberg, A. G. in Food Webs and Biodiversity 181–191 (John Wiley & Sons, 2013).
Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).
Garcia, F. C., Bestion, E., Warfield, R. & Yvon-Durocher, G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc. Natl Acad. Sci. USA 115, 10989–10999 (2018).
Padfield, D., O’Sullivan, H. & Pawar, S. rTPC and nls.multstart: a new pipeline to fit thermal performance curves in R. Methods Ecol. Evol. 12, 1138–1143 (2021).
Acknowledgements
This work was supported by a European Research Council Starting Grant awarded to G.Y.-D. (ERC StG 677278 TEMPDEP). T.C. was supported by the QMEE CDT, funded by NERC grant no. NE/P012345/1. S.P. was funded by Leverhulme Fellowship RF-2020-653\2 and UK national NERC grants NE/M020843/1 and NE/S000348/1.
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G.Y.-D. and S.P. conceived the study. F.C.G. and G.Y.-D. designed the laboratory experiments. F.C.G., R.W. and D.B.O. carried out the laboratory experiments. T.C. and S.P. developed the theory. All authors conducted the analysis of the experimental data and wrote the manuscript.
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García, F.C., Clegg, T., O’Neill, D.B. et al. The temperature dependence of microbial community respiration is amplified by changes in species interactions. Nat Microbiol 8, 272–283 (2023). https://doi.org/10.1038/s41564-022-01283-w
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DOI: https://doi.org/10.1038/s41564-022-01283-w
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