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

Nature Ecology & Evolution volume 3, pages 381–389 (2019)Cite this article

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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.

Authors and 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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  1. Jordan G. Kueneman
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  38. Steven M. Whitfield
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  39. Kelly R. Zamudio
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  40. Ibrahim Zúñiga Chaves
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  41. Douglas C. Woodhams
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  42. Miguel Vences
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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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Supplementary Methods, Supplementary Results, Supplementary Figures 1–12, Supplementary Tables 1–17 and Supplementary References

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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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