Award: OCE-1712134

Award Title: Immunity to Community: Can Quantifying Immune Traits Inform Reef Community Structure?
Funding Source: NSF Division of Ocean Sciences (NSF OCE)
Program Manager: Daniel Thornhill

Outcomes Report

Intellectual Merit Coral diseases have increased significantly throughout the past 30 years. Unhealthy coral reefs cannot support the fish and other life that make the reef a vibrant and diverse ecosystem. Corals reefs in the Caribbean have experienced population collapses due to outbreaks of disease. Importantly, coral species vary in their susceptible to disease, which can lead to a shift in dominant reef species. The reasons behind this variation are unknown. This project directly addressed this question by quantifying coral susceptibility to disease and examining coral immune mechanisms that may drive disease outcomes. Seven species of coral that differ in disease susceptibility, and other life history traits such as growth rate ad morphology were exposed to either active White Plague disease or bacterial immune stimulators. In response to White Plague disease the seven species of corals had one of two treatment outcomes, exposed to disease and not infected or infected, leading to a gradient of susceptible, moderately susceptible and tolerant. The spectrum of disease susceptibility we observed among the coral species corresponded to microbial dysbiosis. This dysbiosis promotes greater disease susceptibility in coral perhaps through different tolerant thresholds for change in the microbiome. Gene expression patterns within each species clustered by species and genotype unless treatment outcome was severe enough (for example O. faveolata, 100% disease prevalence). Additionally, no differentially expressed genes were shared across all seven coral species, indicating that a species-specific response to disease exposure is occurring. While phylogeny influenced gene expression patterns, the response to disease exposure demonstrated consistent immune strategies across all species. For example, NF-kB suppression and inflammation through arachidonate 8-lipoxygenase increased in expression in disease-infected fragments. Genes that significantly increased in disease-exposed coral included inflammation related genes, tyrosine kinase receptor and glycosyl hydrolase. Disease resistance on the other hand, was consistently associated with a stable barrier defense, activation of autophagy and inhibition of apoptosis. We also used five of the seven coral species transcriptomes generated to look for in gene copy number in each species. By coupling these findings with the RNAseq data we show that the genes undergoing rapid evolution exhibit species-specific expression shifts that are enriched for a diversity of biological processes. Interestingly, immune genes are the fastest evolving class of genes demonstrating their importance in the evolutionary history of corals that may lead to differences in disease susceptibility and tolerance that we currently observe on the reef. This project ties all these data together in a novel predictive model of coral community assemblage that incorporates immune traits. Our trait-space model applies an environmental filter (i.e. a white plague outbreak) to a reef community and then uses a hierarchical Bayesian model that incorporates intraspecific trait variation to predict the community assemblage after the environmental filter is applied. Using the data gathered from the first two goals, we identified key immune traits using random forest analyses to determine what traits most influenced the susceptibility group membership. We found genes for signaling in membrane trafficking, cytoskeletal dynamics and cytoskeletal network as well as antioxidants and antimicrobial activity. By applying these traits to our data set we are able to produces post-outbreak relative abundances of the species based on the resistant trait targets that support our observations the resistant species will be the most abundant species after a white plague disease outbreak. Broader Impacts This project supported students at University of Texas, Arlington (Hispanic-serving Institution). Over the funding period, 3 graduate students were directly funded and trained on the award, another 4 benefited indirectly from assisting with field work, and spin-off projects resulting from the large amount of data collected from this award. This award also supported the training of 6 undergraduate students who joined the lab in field work and were mentored by graduate students in the lab. They learned marketable skills such as RNA and DNA extractions, bioinformatic tools and statistical modelling. Many students are pursuing graduate degrees or professional health degrees post-graduation. Public outreach (pre-COVID-19 shutdowns) included booths and coral reef awareness activities at the large EarthX expo in Dallas and local earth day festivals. All Mydlarz lab students all took part in developing activities and interacting with the public at these events, where we estimate engagement with about 4000 people. PI Mydlarz also led several workshops targeting women in science and the concept of sponsorship vs mentorship. To date this award has led to the publication of 10 papers, with one manuscript currently in review and 3 others in a stage of writing and/or development. There were approximately fifteen presentations by graduate and undergraduate students at various conferences. PI Mydlarz co-led a special issue of Frontiers of Immunology, a symposia at the Society of Integrative and Comparative Biology and a session at the 14th International Coral Reef Symposium all related to the topic and data from this award. Last Modified: 03/16/2021 Submitted by: Laura D Mydlarz

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Principal Investigator: Laura D. Mydlarz (University of Texas at Arlington)