CAREER: Holobionts Unfiltered: integrated comparative and experimental examination of the role of cnidarian innate immunity on microbiome structure and stability

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Tropical coral reefs are biodiversity hotspots. For many coastal communities, they are a source of income, a shield against storm damage, and a cultural icon. For more than 240 million years, the growth of stony corals engineered these ecosystems. Over that time, stony corals split into two main groups with more than 1500 species. But corals are not alone; the use of molecular tools identified symbiosis on microscopic scale. Inside each coral polyp are communities of dinoflagellates, bacteria, and archaea that are together called the coral microbiome. Coral microbiomes can help or harm stressed corals. This can affect reef decline due to coral disease and mass coral bleaching. It is thought that coral species with more innate immunity genes have less diverse microbiomes. However, this has not yet been tested. This project will test this idea using a cost-effective ‘genome skimming’ approach to compare coral microbes and immunity genes across 128 coral species. This comparison will suggest how different innate immunity genes shape coral microbiomes. The project will use Karenina, a new statistical method, to test ideas about how immunity changes microbiome dynamics during stress. Finally, the project will test those predictions in laboratory experiments. These research aims are paired with an education plan that will use project data in undergraduate classes, develop a new online interactive bioinformatics textbook, and produce Reef Scenarios, a learning product that will let high school and undergraduate students simulate reef ecology in engaging classroom exercises.The ability of scleractinian (‘stony’) corals to survive many ecological stressors – from macroalgal competition to bleaching – is thought to depend on the outcome of coral x microbe x environment interactions. Therefore, understanding how corals regulate their microbiome is important for understanding coral’s response to environmental stress. Coral innate immunity is thought to play a critical role in regulating the microbiome. Yet the relationship between coral innate immunity and microbiome richness, composition, and stability is not yet well understood. This project implements an integrated research and education plan to study how the evolution of cnidarian innate immunity has influenced microbiome structure, and how changes in the bacterial and archaeal portion of the microbiome may influence survival of thermal stress. This approach will combine a global cross-species survey relating innate immune gene repertoires in diverse coral genomes with their microbiome richness and composition and laboratory experiments in a model cnidarian that can confirm or falsify proposed immunity-microbiome interactions from the survey. A new modeling approach will be used to carefully distinguish competing time-series models of the effects of innate immunity and thermal stress on microbiome dynamics. By uniting sequencing approaches with a tractable cnidarian model system, this project will test key hypotheses in cnidarian host-microbe symbiosis, ecology and evolution. These research objectives are integrated with an education and outreach plan that includes use of project data in undergraduate classes, development of a new interactive online bioinformatics text, and production of Reef Scenarios, a classroom product for simulating reef ecology.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.