Collaborative Research: MIM: Gut-inhabiting fungi influence structure and function of herptile microbiomes through horizontal gene transfer and novel metabolic function

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Reptiles and amphibians are among the most threatened species on the planet, and an increasing number of their species must be managed in captive breeding programs. Understanding the biodiversity and function of microbes that are present in the digestive tracts of reptiles and amphibians is critical for insight into their role in animal health. Early research suggests that the filamentous fungus Basidiobolus is an important member of reptile and amphibian gut microbiomes, and that this fungus influences what types of bacteria are present in the digestive tract. Genomic sequencing of the Basidiobolus fungus shows that genes have been transferred to the fungus from the gut bacteria. This transfer of genes between bacteria and fungi results in novel metabolism in the fungus that may play important roles in regulating the reptile/amphibian host’s immune system, iron metabolism, and chemical communication with the gut bacteria. An interdisciplinary scientific approach will be used to understand the functional roles that specialized metabolites play in microbial interactions between fungi and bacteria in gut microbiomes of animals and also other natural microbiomes. Outreach activities with zoos and the Great Smoky Mountains National Park will share information about reptile and amphibian gut microbiomes with the general public, and educational material will be provided to educators for inclusion in K-12 and university curricula. Interdisciplinary training of students and postdoctoral researchers to prepare them for careers in research, education, and outreach is central to the project. This work will advance a new scientific understanding of the fundamental roles that specialized metabolites play in microbial interactions between fungi and bacteria in gut microbiomes. This will be accomplished through an interdisciplinary approach combining ecology and evolutionary biology, genomics and metagenomics, natural product chemistry, synthetic microbiome experiments, and controlled amphibian feeding trials. Preliminary data reveal that fungi in the genus Basidiobolus are dominant members of the herptile microbiome, and that microbial community structure is shaped by the genetic diversity of Basidiobolus, which has acquired specialized metabolism through HGT. Integration of biological, molecular, genomic, metagenomic, and chemical resources in the proposed herptile system will allow for tests of the following hypotheses: H1: Herptile microbiomes are characterized by unique fungal communities not found in other nonpathogenic, microbiome systems. H2: The bacterial assemblages of herptile microbiomes are structured by interactions with fungi. H3: HGT from co-occurring bacteria to herptile gut fungi allowed Basidiobolus to acquire novel metabolic functions necessary to adapt to, and function in, the herptile microbiome. H4: Fungal-bacterial interactions in herptile GI systems are regulated by metabolites that influence community structure and function. H5: The phenotype of the host-microbiome association is species/context dependent. This work will further refine the general model that the animal gastrointestinal environment promotes HGT between bacteria and fungi, and that this HGT selects for specialized metabolites that modulate the host immune system (cyclic peptides), and allow fungi to function in a reduced oxygen environment and compete in a bacterial rich microbial community (siderophores and surfactins).This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.