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Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas

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Abstract

Animal-associated microbial communities can play major roles in the physiology, development, ecology, and evolution of their hosts, but the study of their diversity has yet focused on a limited number of host species. In this study, we used high-throughput sequencing of partial sequences of the bacterial 16S rRNA gene to assess the diversity of the gut-inhabiting bacterial communities of 212 specimens of tropical anuran amphibians from Brazil and Madagascar. The core gut-associated bacterial communities among tadpoles from two different continents strongly overlapped, with eight highly represented operational taxonomic units (OTUs) in common. In contrast, the core communities of adults and tadpoles from Brazil were less similar with only one shared OTU. This suggests a community turnover at metamorphosis. Bacterial diversity was higher in tadpoles compared to adults. Distinct differences in composition and diversity occurred among gut bacterial communities of conspecific tadpoles from different water bodies and after experimental fasting for 8 days, demonstrating the influence of both environmental factors and food on the community structure. Communities from syntopic tadpoles clustered by host species both in Madagascar and Brazil, and the Malagasy tadpoles also had species-specific isotope signatures. We recommend future studies to analyze the turnover of anuran gut bacterial communities at metamorphosis, compare the tadpole core communities with those of other aquatic organisms, and assess the possible function of the gut microbiota as a reservoir for protective bacteria on the amphibian skin.

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Acknowledgments

Work in Madagascar was made possible by a collaboration accord between the Université d’Antananarivo (Département de Biologie Animale), the Ministère de l’Environnement, des Eaux et Forêts of the Republic of Madagascar, and the Technische Universität Braunschweig. We are grateful to the Malagasy authorities for research and export permits. We are deeply indebted to Otto Larink (TU Braunschweig) for his kind help with identifying the tadpole food items. Meike Kondermann was of invaluable help with lab work. Work in Madagascar was supported by the Volkswagen Foundation to MV, JG, and RDR; by grants of the Deutsche Forschungsgemeinschaft to MV (VE247/2-1 and VE247/9-1) and JG (GL 665/1-1); and by fellowships of the Deutscher Akademischer Austauschdienst to MB and RDR. Maria J. O. Campos and Marcelo de Carvalho authorized our entry into the work area in Itapé, Rio Claro, SP, Brazil. Work in Brazil was supported by a visiting researcher grant of CAPES to MV, CFBH, and ML (88881.062205/2014-01). CFBH thanks grant #2013/50741-7, São Paulo Research Foundation (FAPESP) and CNPq, for a research fellowship. Experiments were approved by the Ethics Committee of UNESP Rio Claro (permit no. 36/2015).

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Authors and Affiliations

  1. Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106, Braunschweig, Germany

    Miguel Vences, Molly C. Bletz, Julia Canitz & Svenja Handreck

  2. Departamento de Zoologia, Instituto de Biociências, UNESP - Univ Estadual Paulista, Campus Rio Claro, Av 24A, N 1515, CEP 13506-900, Rio Claro, SP, Brazil

    Mariana L. Lyra & Célio F. B. Haddad

  3. Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N-122, UCB 334, Boulder, CO, 80309, USA

    Jordan G. Kueneman, Holly M. Archer & Valerie J. McKenzie

  4. Evolutionary Biology and Special Zoology, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany

    Julia Canitz

  5. Visualization Group, Otto-von-Guericke University, Magdeburg, Germany

    Svenja Handreck

  6. Département de Biologie Animale, Université d’Antananarivo, 101, Antananarivo, Madagascar

    Roger-Daniel Randrianiaina

  7. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstrasse 43, 10115, Berlin, Germany

    Ulrich Struck

  8. Department of Genome Analytics, Helmholtz Centre for Infection Research, Braunschweig, Germany

    Sabin Bhuju, Michael Jarek & Robert Geffers

  9. Thünen Institute of Biodiversity, Bundesallee 50, 38116, Braunschweig, Germany

    Christoph C. Tebbe

  10. Department of Animal Ecology and Conservation, University of Hamburg, Martin-Luther-King Platz 3, 20146, Hamburg, Germany

    Julian Glos

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  1. Miguel Vences
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  2. Mariana L. Lyra
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Correspondence to Miguel Vences.

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Communicated by: Sven Thatje

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Vences, M., Lyra, M.L., Kueneman, J.G. et al. Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas. Sci Nat 103, 25 (2016). https://doi.org/10.1007/s00114-016-1348-1

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