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Warming drives ecological community changes linked to host-associated microbiome dysbiosis

Abstract

Anthropogenic climate warming affects many biological systems, ranging in scale from microbiomes to biomes. In many animals, warming-related fitness depression appears more closely linked to changes in ecological community interactions than to direct thermal stress. This biotic community framework is commonly applied to warming studies at the scale of ecosystems but is rarely applied at the scale of microbiomes. Here, we used replicated bromeliad microecosystems to show warming effects on tadpole gut microbiome dysbiosis mediated through biotic community interactions. Warming shifted environmental bacteria and arthropod community composition, with linkages to changes in microbial recruitment that promoted dysbiosis and stunted tadpole growth. Tadpole growth was more strongly associated with cascading effects of warming on gut dysbiosis than with direct warming effects or indirect effects on food resources. These results suggest that assessing warming effects on animal health requires an ecological community perspective on microbiome structure and function.

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Fig. 1: Bromeliad set-up and main experimental findings.
Fig. 2: Piecewise SEMs.

Data availability

Sequence data that support the findings of this study have been deposited in the NCBI Sequence Read Archive with the accession code PRJNA613682. Other data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank R. Bell, T. Bernabe, M. Bletz, T. Jenkinson, R. Martins, D. Medina, W. Neely and R. Salla Jacob. São Paulo Research Foundation (FAPESP) provided grants to M.L.L. (grant no. 2017/26162-8), L.P.R. (grant nos. 2018/23622-0 and 2016/25358-3), L.F.T. (grant nos. 2016/25358-3 and 2019/18335-5), C.F.B.H. (grant no. 2013/50741-7) and G.Q.R. (grant nos. 2017/09052-4 and 2018/12225-0). National Council for Scientific and Technological Development (CNPq) provided research fellowships to L.F.T. (grant no. 300896/2016-6), C.F.B.H. (grant no. 306623/2018-8) and G.Q.R. The Royal Society provided a Newton Advanced Fellowship to G.Q.R. (grant no. NAF\R2\180791).

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C.G.B. and S.E.G. designed the study. All authors carried out the study. C.G.B., S.E.G. and G.Q.R. analysed the data. S.E.G. drafted the manuscript. All authors critically revised the manuscript.

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Correspondence to Sasha E. Greenspan.

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Peer review information Nature Climate Change thanks Obed Hernandez-Gomez and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Greenspan, S.E., Migliorini, G.H., Lyra, M.L. et al. Warming drives ecological community changes linked to host-associated microbiome dysbiosis. Nat. Clim. Chang. 10, 1057–1061 (2020). https://doi.org/10.1038/s41558-020-0899-5

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