Herptile gut microbiomes: a natural system to study multi-kingdom interactions between filamentous fungi and bacteria

Abstract

ABSTRACTReptiles and amphibians (herptiles) represent some of the more endangered and threatened species on the planet and numerous conservation strategies are being implemented with the goal of ensuring species recovery. Little is known, however, about the wild gut microbiome of herptiles and how it relates to the health of wild populations. Here we report results from both a broad survey of hosts and a more intensive sampling of hosts and geography of fungi and bacteria associated with herptile gut microbiomes. We demonstrate that bacterial communities sampled from frogs, lizards and salamanders are structured by the host higher level taxonomy and that the fungusBasidiobolusis a common and natural component of these wild gut microbiomes. Intensive sampling of multiple hosts across the ecoregions of Tennessee revealed that geography and host:geography interactions are strong predictors of distinctBasidiobolusOTUs present within a given host. Co-occurrence analyses ofBasidiobolusand bacterial community diversity supports a correlation and interaction betweenBasidiobolusand bacteria, suggesting thatBasidiobolusmay play a role in structuring the bacterial community. We further the hypothesis that this interaction is advanced by unique specialized metabolism originating from horizontal gene transfer from bacteria toBasidiobolus, and demonstrate thatBasidiobolusis capable of producing a diversity of specialized metabolites including small cyclic peptides.IMPORTANCEThis work significantly advances our understanding of interactions in herptile microbiomes; the role that fungi play as a structural and functional member of herptile gut microbiomes; and the chemical functions that structure host:microbiome phenotypes. We also provide an important observational system of how the gut microbiome represents a unique environment that selects for novel metabolic functions through horizontal gene transfer between fungi and bacteria. Such studies are needed to better understand the complexity of gut microbiomes in nature and will inform conservation strategies for threatened species of herpetofauna.