Award: OCE-1538393

At a global scale, coral reef ecosystems are declining, due in large part to the expanding scale of human activities: overexploiting algal-grazing reef fish, increasing the loads of sediment and nutrients in watersheds upslope of reefs and changing the fundamental thermal and chemical properties of the water in which corals live. This degradation, specifically the loss of live coral, is associated with a phase shift towards a system dominated by fleshy algae. In addition to the direct impacts of fleshy algae outcompeting calcareous reef-building organisms, algal exudates facilitate the growth of microbes (e.g., bacteria and viruses) at the expense of the larger macro-organisms in a process called microbialization. This process is widespread in human-impacted coastal ecosystems altering ecosystem biogeochemistry and trophic structure such that energy flow is reallocated toward bacteria and viruses instead of toward higher trophic levels. While the anthropogenic processes driving the spread of algae are multiple and synergistic, reef resilience to these stressors is poorly understood, and determining the underlying processes of microbialization is critical for future management efforts. This NSF funded project integrated research on the geochemistry of dissolved organic matter, microbial genomics and ecosystem process measurements to test hypothetical mechanisms by which microbially-mediated feedbacks facilitate the spread of fleshy algae on Pacific reef ecosystems. Over the course of this project, presented in more than 30 oral and poster conference abstracts and 16 peer-reviewed journal articles, we detailed the effects of nutrient enrichment on coral physiology, coral reef producer DOM and ecosystem function, characterized metabolites via NMR and MS/MS from a variety of reef organisms, explored the community metagenomics of diel and spatial patterns in coral reef microbes, and examined the island mass effect on plankton and biogeochemistry around French Polynesia. In one significant paper published in Nature Microbiology we surveyed the genomics of microbes and the quantities of dissolved organic matter in coral reefs around the globe to explore the changes in community structure and bacterial gene functions associated with algal phase shifts. In another paper published in Nature Communications we demonstrated the planktonic microbial community changes in taxonomic composition and gene expression that occur over a diel cycle at pristine reefs located in the central Pacific. We conducted long term chronic nutrient enrichment experiments on corals and algae, demonstrating how they shifted their physiology, growth, and organic matter exudation rates and showed how that impacted the overall photosynthetic production balance of a model coral reef ecosystem. With collaborators at Scripps Institution of Oceanography and the University of California, San Diego, we developed a pipeline to characterize coral reef derived organic materials (exometabolites) using tandem mass spectrometry (LC-MS/MS). We found that the different primary producers inhabiting coral reef ecosystem, i.e., diverse assemblages of corals and macroalgae, exude hundreds of dissolved compounds that are chemically distinct between organisms (Fig 3). These finding lend to a deeper, mechanistic understanding of how the proportion of macroorganisms – corals versus fleshy algae – present on the reef benthos can determine the structure of microbial communities that consume them. A key product of this research is the broader understanding of how the composition of corals and algae on reefs interact synergistically with complex microbial communities to influence reef ecosystem resilience in the face of global change. The project was conducted within the Moorea Coral Reef LTER program, leveraging a wealth of time series data on multiple reef habitats as well as contextualizing our in situ sampling with ongoing physical, geochemical and biological monitoring programs. Finally, our research contributed to marine conservation and the monitoring US reefs through a collaboration with the National Oceanic and Atmospheric Administration (NOAA). We incorporated several of the project’s objectives on cruises to the North West and Main Hawaiian Islands, American Samoa, the Mariana Archipelago, and the Pacific Remote Island Areas. This partnership allowed for the integration of the comprehensive monitoring efforts facilitated by NOAA with our molecular approaches to characterize the microbial and chemical composition of coral reef ecosystems and provide a holistic understanding of coral reef function across the entire US pacific. Last Modified: 02/28/2021 Submitted by: Craig E Nelson