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Community richness of amphibian skin bacteria correlates with bioclimate at the global scale

Abstract

Animal-associated microbiomes are integral to host health, yet key biotic and abiotic factors that shape host-associated microbial communities at the global scale remain poorly understood. We investigated global patterns in amphibian skin bacterial communities, incorporating samples from 2,349 individuals representing 205 amphibian species across a broad biogeographic range. We analysed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global amphibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more diverse skin microbiomes in environments with colder winters and less stable thermal conditions compared with environments with warm winters and less annual temperature variation. We used bioinformatically predicted bacterial growth rates, dormancy genes and antibiotic synthesis genes, as well as inferred bacterial thermal growth optima to propose mechanistic hypotheses that may explain the observed patterns. We conclude that temporal and spatial characteristics of the host’s macro-environment mediate microbial diversity.

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Data availability

A full description of data analyses is provided in the Supplementary Information. Data for all newly sequenced samples is available on the Short Read Archive (Bioproject PRJNA474496). All figures include associated raw data and there are no restrictions on data availability. Correspondence and requests for materials should be addressed to M.V. or D.C.W.

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Acknowledgements

This study was supported by grants of National Science Foundation (DEB-1146284 to V.J.M.; IOS-1121758 to L.R.-S.; DEB-1310036 to A.V.L.), Templeton Foundation to V.J.M., Deutsche Forschungsgemeinschaft (DFG) to M.V. (VE247/9-1), CAPES to M.V. and C.F.B.H., FAPESP (#2013/50741-7) and CNPq to C.F.B.H., Simons Foundation (429440, WTW) to J.G.K., Deutscher Akademischer Austauschdienst (DAAD) to M.C.B., University of Costa Rica (Project 801-B2-029) and Costa Rican Ministry of Science and Technology (849-PINN-2015)-I to J.G.A., the Portuguese National Funds through FCT (Exploratory Research Project: IF/00209/2014/CP1256/CT0011) to A.C. and the National Research Foundation of Korea (2015R1D1A1A01057282) to B.W. We are indebted to M. Kondermann for her assistance with laboratory work, A. Borzee, R. Kakehashi and T. Kosch for their support in sample collection, and the Organization for Tropical Studies, La Selva Biological Station and G. Alvarado for field support in Costa Rica. All new sampling was done with the appropriate permits of national authorities, where required; in Costa Rica, of the Institutional Biodiversity Commission of the University of Costa Rica (Resolution 371 014) and the Costa Rican Ministry of Environment and Energy (Resolution 091-2012-SINAC).

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J.G.K., M.C.B., V.J.M., D.C.W. and M.V. conceived the study, coordinated the analyses and wrote the manuscript. J.G.K., M.C.B., D.C.W., G.B. and M.J. designed and performed data analysis. J.G.A., A.B., M.B., L.B., A.C., C.F.B.H., R.N.H., W.H., M.H., J.L.K., J.K., A.K., A.L., A.H.L., D.M., J.J.N., R.G.B.P., A.P.T., F.C.E.R., E.A.R., A.R., L.R.S., G.V.A., B.W., J.B.W., S.M.W., K.Z., I.Z.C. contributed materials and data. H.A., L.A., R.G. and M.J. performed laboratory work. P.J.K., R.S. and C.C.T. contributed to data analysis. All authors contributed to the development and revision of the manuscript.

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Correspondence to Douglas C. Woodhams or Miguel Vences.

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Kueneman, J.G., Bletz, M.C., McKenzie, V.J. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat Ecol Evol 3, 381–389 (2019). https://doi.org/10.1038/s41559-019-0798-1

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