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).

Author information

Author notes

  1. These authors have contributed equally: Jordan G. Kueneman, Molly C. Bletz.

Affiliations

  1. Smithsonian Tropical Research Institute, Panama City, Republic of Panama

    • Jordan G. Kueneman
    •  & Douglas C. Woodhams
  2. Department of Biology, University of Massachusetts Boston, Boston, MA, USA

    • Molly C. Bletz
    • , Robert Stevenson
    •  & Douglas C. Woodhams
  3. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

    • Valerie J. McKenzie
    • , Holly Archer
    •  & Ana Lisette Arellano
  4. Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA

    • C. Guilherme Becker
  5. Earth Lab, University of Colorado, Boulder, CO, USA

    • Maxwell B. Joseph
  6. Center for Research in Microscopic Structures, University of Costa Rica, San José, Costa Rica

    • Juan G. Abarca
    • , Adrián Pinto-Tomás
    • , Gabriel Vargas Asensio
    •  & Ibrahim Zúñiga Chaves
  7. School of Biological Sciences, Seoul National University, Seoul, South Korea

    • Arnaud Bataille
    •  & Bruce Waldman
  8. Department of Biology and Chemistry, Liberty University, Lynchburg, VA, USA

    • Matthew Becker
  9. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    • Lisa K. Belden
    •  & Daniel Medina
  10. CIBIO, Research Centre in Biodiversity and Genetic Resources, Universidade do Porto, Vairao, Portugal

    • Angelica Crottini
  11. Department of Genome Analytics, Helmholtz Centre for Infection Research, Braunschweig, Germany

    • Robert Geffers
    •  & Michael Jarek
  12. Departamento de Zoologia e Centro de Aquicultura, I.B., UNESP, Rio Claro, SP, Brazil

    • Célio. F. B. Haddad
  13. Department of Biology, James Madison University, Harrisonburg, VA, USA

    • Reid N. Harris
  14. Department of Pathology, Microbiology and Immunology, Vanderbilt University School of Medicine, Nashville, TN, USA

    • Whitney M. Holden
    •  & Louise Rollins-Smith
  15. Department of Biology, Vassar College, Poughkeepsie, NY, USA

    • Myra Hughey
  16. Department of Biology, Tufts University, Medford, MA, USA

    • Patrick J. Kearns
  17. Biology Department, University of South Dakota, Vermillion, SD, USA

    • Jacob L. Kerby
  18. Department of Biology, University of Copenhagen, and Center for Macroecology, Evolution and Climate Natural History Museum of Denmark, Copenhagen, Denmark

    • Jos Kielgast
  19. Department of Bio-Science, Nagahama Institute of Bio-Science and Technology, Nagahama, Japan

    • Atsushi Kurabayashi
  20. Amphibian Research Center, Hiroshima University, Higashi-Hiroshima, Japan

    • Atsushi Kurabayashi
  21. Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    • Atsushi Kurabayashi
  22. Department of Biology, University of Florida, Gainesville, FL, USA

    • Ana V. Longo
  23. Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    • Andrew Loudon
  24. Conservation and Science, Cleveland Metroparks Zoo, Cleveland, OH, USA

    • Andrew Loudon
  25. Institute of Marine and Limnological Sciences, Sciences Faculty, Universidad Austral de Chile, Valdivia, Chile

    • José J. Nuñez
  26. School of Marine Sciences, Ruppin Academic Center, Mikhmoret, Israel

    • R. G. Bina Perl
  27. Biochemistry Department, School of Medicine; Center for Research in Cell and Molecular Biology and Center for Research in Microscopic Structures, University of Costa Rica, San José, Costa Rica

    • Adrián Pinto-Tomás
  28. Department of Animal Biology, University of Antananarivo, Antananarivo, Madagascar

    • Falitiana C. E. Rabemananjara
  29. Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico

    • Eria A. Rebollar
  30. Institute of Zoology, Tierärztliche Hochschule Hannover, Hannover, Germany

    • Ariel Rodríguez
  31. Thünen Institute of Biodiversity, Braunschweig, Germany

    • Christoph C. Tebbe
  32. Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA

    • Bruce Waldman
  33. Department of Biology, Eastern Washington University, Cheney, WA, USA

    • Jenifer B. Walke
  34. Conservation and Research Department, Zoo Miami, Miami, FL, USA

    • Steven M. Whitfield
  35. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA

    • Kelly R. Zamudio
  36. Zoologisches Institut, Technische Universität Braunschweig, Braunschweig, Germany

    • Miguel Vences

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Contributions

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.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Douglas C. Woodhams or Miguel Vences.

Supplementary information

  1. Supplementary Information

    Supplementary Methods, Supplementary Results, Supplementary Figures 1–12, Supplementary Tables 1–17 and Supplementary References

  2. Reporting Summary

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DOI

https://doi.org/10.1038/s41559-019-0798-1

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