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Microbiota and skin defense peptides may facilitate coexistence of two sympatric Andean frog species with a lethal pathogen

The ISME Journalvolume 13pages361373 (2019) | Download Citation

Abstract

Management of hyper-virulent generalist pathogens is an emergent global challenge, yet for most disease systems we lack a basic understanding as to why some host species suffer mass mortalities, while others resist epizootics. We studied two sympatric species of frogs from the Colombian Andes, which coexist with the amphibian pathogen Batrachochytrium dendrobatidis (Bd), to understand why some species did not succumb to the infection. We found high Bd prevalence in juveniles for both species, yet infection intensities remained low. We also found that bacterial community composition and host defense peptides are specific to amphibian life stages. We detected abundant Bd-inhibitory skin bacteria across life stages and Bd-inhibitory defense peptides post-metamorphosis in both species. Bd-inhibitory bacteria were proportionally more abundant in adults of both species than in earlier developmental stages. We tested for activity of peptides against the skin microbiota and found that in general peptides did not negatively affect bacterial growth and in some instances facilitated growth. Our results suggest that symbiotic bacteria and antimicrobial peptides may be co-selected for, and that together they contribute to the ability of Andean amphibian species to coexist with the global pandemic lineage of Bd.

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Acknowledgements

This study was partially completed with financial support from The Rufford Foundation (RSG15305-1 to S.V.F.), Sciences Faculty at Universidad de los Andes (Proyecto Semilla to S.V.F.), the National Science Foundation (1258133 & 1633948 to V.T.V.). J.G.K. was supported by the University of Massachusetts Boston and the Simons Foundation (429440, WTW). We thank COLCIENCIAS for supporting doctoral studies of S.V.F. A.A.G. was a recipient of “Es Tiempo de volver 2015–2016” postdoctoral fellowship from COLCIENCIAS and the Universidad de La Sabana (Bogotá, Colombia). Procedures for handling animals were approved by the Colombian National Authority under resolution N°0528. For assistance in the field, we thank L.M. Arenas, J. Méndez-Narvaez, P. Palacios, C. Rodríguez, C.M. Betancourth, A. Paz, E. Lasso, R. Márquez, M.E. Cárdenas, E.M. Medina, C. Esquivel, M. González, A.J. Crawford, J.A. Hernández, M. Guevara, C. Sarmiento, M. Anganoy, A. Zarling, J. Sunyer, and D. Galindo. We thank Mr. Mauricio Moreno for allowing us to work at his property. For help in the laboratory, we thank S. Ellison, T. Nguyen, and B. LaBumbard, and for analysis advice, we thank M. Bletz.

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Author notes

    • Sandra V. Flechas

    Present address: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia

Affiliations

  1. Department of Biological Sciences, Universidad de los Andes, Bogotá, 111711, Colombia

    • Sandra V. Flechas
    •  & Adolfo Amézquita
  2. Faculty of Engineering, Universidad de la Sabana, Chía, AA, 53753, Colombia

    • Alejandro Acosta-González
  3. Department of Microbiology, Faculty of Sciences, Pontificia Universidad Javeriana, Bogotá, AA 56710, Colombia

    • Laura A. Escobar
    • , Zilpa Adriana Sánchez-Quitian
    •  & Claudia M. Parra-Giraldo
  4. Biology Department, University of Massachusetts Boston, Boston, MA, 02125, USA

    • Jordan G. Kueneman
    •  & Douglas C. Woodhams
  5. Smithsonian Tropical Research Institute, Panama, Apartado 0843-03092, Republic of Panama

    • Jordan G. Kueneman
    •  & Douglas C. Woodhams
  6. Environmental Management Group, Department of Biology and Microbiology, Universidad de Boyacá, Tunja, 150000003, Colombia

    • Zilpa Adriana Sánchez-Quitian
  7. Department of Pathology, Microbiology and Immunology, Vanderbilt University, School of Medicine, Nashville, TN, 37232, USA

    • Louise A. Rollins-Smith
    •  & Laura K. Reinert
  8. Department of Biology, San Francisco State University, San Francisco, CA, 94132-1722, USA

    • Vance T. Vredenburg

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The authors declare that they have no conflict of interest.

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Correspondence to Sandra V. Flechas.

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https://doi.org/10.1038/s41396-018-0284-9