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Variation in the Slimy Salamander (Plethodon spp.) Skin and Gut-Microbial Assemblages Is Explained by Geographic Distance and Host Affinity

  • Host Microbe Interactions
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Abstract

A multicellular host and its microbial communities are recognized as a metaorganism—a composite unit of evolution. Microbial communities have a variety of positive and negative effects on the host life history, ecology, and evolution. This study used high-throughput amplicon sequencing to characterize the complete skin and gut microbial communities, including both bacteria and fungi, of a terrestrial salamander, Plethodon glutinosus (Family Plethodontidae). We assessed salamander populations, representing nine mitochondrial haplotypes (‘clades’), for differences in microbial assemblages across 13 geographic locations in the Southeastern United States. We hypothesized that microbial assemblages were structured by both host factors and geographic distance. We found a strong correlation between all microbial assemblages at close geographic distances, whereas, as spatial distance increases, the patterns became increasingly discriminate. Network analyses revealed that gut-bacterial communities have the highest degree of connectedness across geographic space. Host salamander clade was explanatory of skin-bacterial and gut-fungal assemblages but not gut-bacterial assemblages, unless the latter were analyzed within a phylogenetic context. We also inferred the function of gut-fungal assemblages to understand how an understudied component of the gut microbiome may influence salamander life history. We concluded that dispersal limitation may in part describe patterns in microbial assemblages across space and also that the salamander host may select for skin and gut communities that are maintained over time in closely related salamander populations.

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Data Accessibility

All raw sequence data has been submitted to GenBank SRA under the accession number PRJNA590016.

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Acknowledgments

DMW would like to thank Michael Edelbrock, Brandon Edelbrock, Julia Edelbrock, Brandy Lawrence, Michael McAndrew, Ingrid Godfrey, Jeff Miller, and Dakota Esterline for assistance on research trips.

Author information

Authors and Affiliations

  1. Department of Biology, Middle Tennessee State University, PO Box 60, Murfreesboro, TN, 37132, USA

    Donald M. Walker, Matthew Grisnik, Alexander Romer & Alejandro Grajal-Puche

  2. Department of Biology, Tennessee Technological University, 1100 N. Dixie Ave, Cookeville, TN, 38505, USA

    Aubree J. Hill

  3. Department of Biology, East Carolina University, Greenville, NC, 27858, USA

    Molly A. Albecker & Michael W. McCoy

  4. Department of Biology, Piedmont College, 1021 Central Avenue, Demorest, GA, 30535, USA

    Carlos Camp & Jessica Wooten

  5. Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Ancon, Panama, Republic of Panama

    Crystal Kelehear

  6. Department of Biology, Geology and Physical Sciences, Sul Ross State University, Alpine, TX, 79832, USA

    Crystal Kelehear & Sean P. Graham

  7. Department of Natural Sciences, The University of Findlay, 1000 N. Main St, Findlay, OH, 45840, USA

    Justin Rheubert

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  1. Donald M. Walker
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Contributions

DMW, SPG, CK, JW, CC conceived the study. DMW, SPG, CK, CC, JR collected specimens and contributed to field work. JW sequenced the salamander specimens, DMW ran the bioinformatics analyses, and MA, MM, MG, AG, AR ran the statistical analyses. DMW, SPG, CK, AJH, MG, AG, AR wrote the manuscript and all authors contributed equally to revisions.

Corresponding author

Correspondence to Donald M. Walker.

Ethics declarations

Tennessee Technological University research policies and guidelines for the ethical treatment of animals were followed during this study (TTU-IACUC—15-16—001). Research collection permits were obtained from the appropriate governmental organizations (CHE901200, 14-SC00873, TWRA3886, AL2014044693068680, AL2016021753868680, 29-WJH-16-184, MS0722163).

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Supplementary Table 1

Salamander specimen collection data. (XLSX 13 kb)

Supplemental Figure 1

Nuclear RPL12 maximum likelihood gene tree. (PDF 2 kb)

Supplemental Figure 2

Complete mitochondrial (cytb) tree. (PDF 29 kb)

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Walker, D.M., Hill, A.J., Albecker, M.A. et al. Variation in the Slimy Salamander (Plethodon spp.) Skin and Gut-Microbial Assemblages Is Explained by Geographic Distance and Host Affinity. Microb Ecol 79, 985–997 (2020). https://doi.org/10.1007/s00248-019-01456-x

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  • DOI: https://doi.org/10.1007/s00248-019-01456-x

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