Abiotic stress alters nitrogen metabolism and disrupts the coral holobiont

Metabolic symbiotic exchange, the transfer of small metabolic precursors and photosynthate products between the eukaryotic dinoflagellate algal endosymbiont belonging to the family Symbiodiniaceae and coral cnidarian hosts, is what ungirds the success of Scleractinian (reef-building) corals. Symbiodiniaceae use photic energy to perform key biochemical and nutrient assimilation processes including carbon fixation, respiration, nitrogen assimilation, and metabolite biosynthesis that are translocated to the host. Warming ocean temperatures resulting from anthropogenic climate change disrupts this relationship leading to coral starvation, a process colloquially known as coral bleaching, whereby Symbiodiniaceae are expelled from the tissues of the host organism. This has contributed to a precipitous loss of coral reef cover worldwide and threatens to worsen over the next several decades. Coral resilience hinges on understanding the metabolic changes that precipitate dysbiosis and understanding whether they are algal or host derived. Using omics techniques, it has been shown that changes in nitrogen rich short peptides strongly correlate to heat stress. In this dissertation, I further investigate the impact of heat stress on the nitrogen metabolism in the coral holobiont through metaorganism and culture-based experiments. Using stable isotope tracing, I show that ¹⁵NH₄⁺ is rapidly assimilated into the metabolomes of three coral species endemic to the Hawaiian Reef Montipora capitata, Porites compressa, and Pocillopora acuta and incorporated into dipeptide pools are ambient temperature. Also, in a population wide study (n=900) across Kāne'ohe Bay, O'ahu, I explore the conserved nature of stress responses across coral populations of Montipora capitata and Pocillopora acuta, two species that have differing genetic and reproductive strategies. In this study I identify several additional putative di-, tri-, and tetrapeptide products that are synthesized in response to stress that decrease during a recovery period. This work showed that the stress response among these two coral species is quite synergistic despite them having distinct genetic and reproductive strategies. Finally, I demonstrate that abiotic stress factors of temperature and light shift the metabolome of Cladocopium algal symbionts and associated bacterial populations in culture. This work demonstrates that temperature is the main driver of stress across the coral microbiome as shifting from photosynthesis to respiration at low light does not induce stress correlated metabolite enrichment.