Prokaryotes and Partners: Exploring How Microbe – Organic Matter Interactions Inform Carbon Cycling in Healthy and Degraded Coral Reefs

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2023
Authors
Sparagon, Wesley James
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Nelson, Craig E.
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Marine Biology
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Coral reefs are a paradox: these vibrant ecosystems maintain high levels of gross primary production and biomass, all while bathed in resource-poor waters. A longstanding hypothesis is that these properties are the result of efficient recycling of organic carbon and nutrients, partially underpinned by the interaction between microbes and organic matter (OM). Microbe-OM interactions occur in both organism-associated and free-living compartments on coral reefs, and the outcome of these interactions dictates the flow of carbon and nutrients through the food web. In this dissertation, I explore how microbe-OM interactions support the tight recycling of carbon on coral reefs in both organism-associated and free-living forms, and how these interactions may shift as coral reefs change. Specifically, I examined 1) the succession of microbes and metabolites as algal biomass is digested in the gut of nenue (Kyphosus spp.), an herbivorous Hawaiʻian reef fish, 2) the impacts of changing benthic primary producers on the carbon cycling capabilities of reef bacterioplankton and 3) how thermal stress induced bleaching alters coral OM release into the water column and the subsequent bacterioplankton response. In nenue, associations between microbes and metabolites continuously shifted through the gut as macroalgal biomass was digested: bile acid deconjugation associated with early gut microbiota, small peptide production associated with midgut microbiota, and phospholipid production associated with hindgut microbiota. In the coral reef water column, shifts in abundance of benthic primary producers from corals to algae had a dramatic effect on microbe-DOM (dissolved organic matter) interactions and carbon cycling. Coral-associated bacterioplankton grew significantly more efficiently and to significantly lower abundances than algal-associated bacterioplankton, with growth efficiencies ranging from 3% in algal-associated bacterioplankton to 50% in coral-associated bacterioplankton. This suggests that bacterioplankton switch from acting as trophic links for carbon transfer to trophic sinks as reefs undergo coral-algal phase shifts. Change in sea surface temperatures can also have dramatic impacts on the water column via altered DOM exudation from thermally stressed and bleaching corals. Controlled aquaria and bottle incubations revealed that thermal stress and bleaching altered coral DOM exudate quantity and composition, yielding upwards of 3x DOC release from corals and DOM with distinct metabolomic compositions. These DOM exudates in turn yielded a 2-fold increase in microbial loads and altered microbial community structure, driven by a significant enrichment of copiotrophic and putatively pathogenic bacterial taxa. Together the work comprising this dissertation collectively points to the critical role microbe-OM interactions have in mediating carbon flow in coral reefs, and how environmental changes may fundamentally shift these interactions and alter coral reef ecosystem function.
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Biological oceanography, Microbiology, bacterioplankton, coral reefs, dissolved organic matter, microbial ecology
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