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Variation of the Frog Skin Microbiota Across an Environmental Gradient: Taxonomic Diversity and Potential Function

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Variation of the Frog Skin Microbiota Across an Environmental Gradient: Taxonomic Diversity and Potential Function VARIATION OF THE FROG SKIN MICROBIOTA ACROSS AN ENVIRONMENTAL GRADIENT: TAXONOMIC DIVERSITY AND POTENTIAL FUNCTION Brandon J. Varela Department of Biology, Neotropical Environment Option McGill University, Montreal August, 2017 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Master’s in Science in Biology Brandon J. Varela, 2017 1 TABLE OF CONTENTS ABSTRACT .............................................................................................................. 4 RÉSUMÉ .................................................................................................................. 5 ACKNOWLEDGEMENTS ...................................................................................... 7 CONTRIBUTIONS OF AUTHORS ......................................................................... 9 Introduction ............................................................................................................ 10 Thesis objectives ......................................................................................................................... 14 Hypothesis 1 ........................................................................................................................................ 15 Hypothesis 2 ........................................................................................................................................ 15 Hypothesis 3 ........................................................................................................................................ 16 Materials and Methods ........................................................................................... 17 Sampling sites and frog species ................................................................................................... 17 DNA extraction, Bd analyses and 16S rRNA library preparation ............................................... 19 Sequence reads processing .......................................................................................................... 21 Comparing alpha and beta diversity ........................................................................................... 21 Comparing bacterial diversity and functional group variation ................................................... 23 Estimating the Bd-inhibiting and Bd-enhancing functions of the skin microbiota ....................... 25 Results .................................................................................................................... 26 Frog host comparison ................................................................................................................. 26 Soil pH, onset of the wet season and site differences ................................................................... 27 Skin microbiota potential function variation .............................................................................. 29 Variation of potential Bd-interacting microbiota ........................................................................ 30 Bd diagnosis ................................................................................................................................ 31 Discussion ............................................................................................................... 32 Influence of soil pH on skin microbiota ....................................................................................... 32 Influence of the onset of the wet season on skin microbiota ........................................................ 33 Functional groups associated with the skin microbiota ............................................................... 34 Microbial diversity and functional group richness ...................................................................... 37 Conclusion .............................................................................................................. 39 Literature cited ....................................................................................................... 41 Tables ..................................................................................................................... 54 Table 1. Host species habitat and sample sizes of the three dendrobatid frogs by life stage. ....... 54 Table 2. Abiotic factors for the sites sampled along the Panama Canal: soil pH, volume of precipitation (mm) accumulated 5, 10, 15 days before sampling and historic annual mean......... 55 Table 3. Bacterial functional groups that best defined the site differences in functions and their corresponding linear discriminant analysis (LDA) scores computed using LEfSe. ...................... 56 Figures .................................................................................................................... 57 2 Figure 1. Map of sampling sites along the Panama Canal. A steep precipitation gradient separates the drier-Pacific Coast (Cerro Ancón) from the wetter-Atlantic Coast (Fort Sherman). .................................................................................................................................................... 57 Figure 2. Skin bacterial alpha diversity comparison between three dendrobatid frog species. ... 58 Figure 3. Bacterial Operational Taxonomic Units (OTUs) that best define bacterial community structure differences between sites, frog species, and in relation to the onset of the wet season. .. 59 Figure 4. Patterns of frog skin bacterial alpha variation across sites in D. auratus (A) and beta diversity variation across sites in three dendrobatid frogs (B). ................................................... 60 Figure 5. Frog skin bacterial alpha (A) and beta (B) diversity before and after the onset of the wet season. .................................................................................................................................. 61 Figure 6. Mean relative abundance of skin microbial functional groups before and after the onset of the wet season (A). ......................................................................................................... 62 Figure 7. The proportion of Batrachochytrium dendrobatidis (Bd)-interacting microbiota across sites in D. auratus (A, B) and in relation to the onset of the wet season in three dendrobatid frog species (C, D). ............................................................................................................................. 63 APPENDICES ........................................................................................................ 64 3 ABSTRACT Research on the amphibian skin microbiota has focused on identifying bacterial taxa that deter a pathogenic chytrid fungus (Batrachochytrium dendrobatidis - Bd), and on describing patterns of microbiota variation. However, it remains unclear how environmental variation affects amphibian skin bacterial communities, and whether the overall functional diversity of the amphibian skin microbiota is associated to such variation. I sampled skin microbial communities from three dendrobatid frog species before and after the onset of the wet season in one site, and from one dendrobatid frog species across an environmental gradient along the Panama Canal. I found frog skin microbial alpha diversity to be highest in frogs from sites with low soil pH, but no clear effect of the onset of the wet season. However, I found frog skin microbial community structure (beta diversity) to be affected by soil pH and the onset of the wet season, which also resulted in a decrease of between-samples variation. Across the sampled frog species, bacterial functional groups changed with the onset of the wet season, with certain bacterial functional groups entirely disappearing and others differing in their relative abundances after the onset of the wet season. In particular, I found proportion of Bd-inhibiting bacteria to correlate with mean soil pH, and to increase in two of the frog species with the onset of the wet season. Taken together, my results suggest that the host’s requirements facilitated by bacteria, including disease resistance, may be site-specific and follow seasonal patterns. These new insights should be considered when implementing conservation programs that include a probiotic bacteria treatment. 4 RÉSUMÉ La recherche sur le microbiote de la peau des amphibiens a pris plusieurs chemins dans les dernières années. Elle s’est principalement concentrée sur l’identité des bactéries dissuadant le champignon pathogène chytride (Batrachochytrium dendrobatidis - Bd) et sur la description de la variation du microbiote. Toutefois, il n’est pas encore clair comment la variation environnementale affecte la communauté bactérienne sur la peau des amphibiens. De plus, on s’interroge encore sur la diversité fonctionnelle du microbiote associée à une telle variation environnementale. J’ai échantillonné la communauté microbienne cutanée de trois espèces de grenouille de la famille Dendrobathidae avant et après le début de la saison humide. J’ai également échantilloné la communauté microbienne cutanée d’une espèce de Dendrobathidae à travers un gradient environnemental le long du canal de Panama. J’ai trouvé que la diversité alpha de la communauté microbienne cutanée était plus grande entre les grenouilles provenant de sites où le site avait un pH bas. Cependant, il n’y avait pas d’effet clair par rapport au début de la saison humide. Toutefois, j’ai trouvé que la structure de la communauté microbienne (la diversité béta) était affectée par le
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