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High molecular weight (HMW; >1 kDa) carbohydrates are a major component of dissolved organic matter (DOM) released by benthic primary producers. Despite shifts from coral to algae dominance on many reefs, little is known about the effects of exuded carbohydrates on bacterioplankton communities in reef waters. We compared the monosaccharide composition of HMW carbohydrates exuded by hard corals and brown macroalgae and investigated the response of the bacterioplankton community of an algae-dominated Caribbean reef to the respective HMW fractions. HMW coral exudates were compositionally distinct from the ambient, algae-dominated reef waters and similar to coral mucus (high in arabinose). They further selected for opportunistic bacterioplankton taxa commonly associated with coral stress (i.e.,Rhodobacteraceae,Phycisphaeraceae,Vibrionaceae, andFlavobacteriales) and significantly increased the predicted energy-, amino acid-, and carbohydrate-metabolism by 28%, 44%, and 111%, respectively. In contrast, HMW carbohydrates exuded by algae were similar to those in algae tissue extracts and reef water (high in fucose) and did not significantly alter the composition and predicted metabolism of the bacterioplankton community. These results confirm earlier findings of coral exudates supporting efficient trophic transfer, while algae exudates may have stimulated microbial respiration instead of biomass production, thereby supporting the microbialization of reefs. In contrast to previous studies, HMW coral and not algal exudates selected for opportunistic microbes, suggesting that a shift in the prevalent DOM composition and not the exudate type (i.e., coral vs algae)per se, may induce the rise of opportunistic microbial taxa. IMPORTANCEDissolved organic matter (DOM) released by benthic primary producers fuels coral reef food webs. Anthropogenic stressors cause shifts from coral to algae dominance on many reefs, and resulting alterations in the DOM pool can promote opportunistic microbes and potential coral pathogens in reef water. To better understand these DOM-induced effects on bacterioplankton communities, we compared the carbohydrate composition of coral- and macroalgae-DOM and analyzed the response of bacterioplankton from an algae-dominated reef to these DOM types. In line with the proposed microbialization of reefs, coral-DOM was efficiently utilized, promoting energy transfer to higher trophic levels, whereas macroalgae-DOM likely stimulated microbial respiration over biomass production. Contrary to earlier findings, coral- and not algal-DOM selected for opportunistic microbial taxa, indicating that a change in the prevalent DOM composition, and not DOM type, may promote the rise of opportunistic microbes. Presented results may also apply to other coastal marine ecosystems undergoing benthic community shifts. 

Abstract Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events. 

Reef-building crustose coralline algae (CCA) are known to facilitate the settlement and metamorphosis of scleractinian coral larvae. In recent decades, CCA coverage has fallen globally and degrading environmental conditions continue to reduce coral survivorship, spurring new restoration interventions to rebuild coral reef health. In this study, naturally produced chemical compounds (metabolites) were collected from two pantropical CCA genera to isolate and classify those that induce coral settlement. In experiments using four ecologically important Caribbean coral species, we demonstrate the applicability of extracted, CCA-derived metabolites to improve larval settlement success in coral breeding and restoration efforts. Tissue-associated CCA metabolites induced settlement of one coral species,Orbicella faveolata, while metabolites exuded by CCA (exometabolites) induced settlement of three species:Acropora palmata,Colpophyllia natansandOrbicella faveolata. In a follow-up experiment, CCA exometabolites fractionated and preserved using two different extraction resins induced the same level of larval settlement as the unfractionated positive control exometabolites. The fractionated CCA exometabolite pools were characterized using liquid chromatography tandem mass spectrometry, yielding 145 distinct molecular subnetworks that were statistically defined as CCA-derived and could be classified into 10 broad chemical classes. Identifying these compounds can reveal their natural prevalence in coral reef habitats and facilitate the development of new applications to enhance larval settlement and the survival of coral juveniles. 

One mechanism giving fleshy algae a competitive advantage over corals during reef degradation is algal-induced and microbially-mediated hypoxia (typically less than 69.5 µmol oxygen L −1 ). During hypoxic conditions oxygen availability becomes insufficient to sustain aerobic respiration in most metazoans. Algae are more tolerant of low oxygen conditions and may outcompete corals weakened by hypoxia. A key question on the ecological importance of this mechanism remains unanswered: How extensive are local hypoxic zones in highly turbulent aquatic environments, continuously flushed by currents and wave surge? To better understand the concert of biological, chemical, and physical factors that determine the abundance and distribution of oxygen in this environment, we combined 3D imagery, flow measurements, macro- and micro-organismal abundance estimates, and experimentally determined biogenic oxygen and carbon fluxes as input values for a 3D bio-physical model. The model was first developed and verified for controlled flume experiments containing coral and algal colonies in direct interaction. We then developed a three-dimensional numerical model of an existing coral reef plot off the coast of Curaçao where oxygen concentrations for comparison were collected in a small-scale grid using fiberoptic oxygen optodes. Oxygen distribution patterns given by the model were a good predictor for in situ concentrations and indicate widespread localized differences exceeding 50 µmol L -1 over distances less than a decimeter. This suggests that small-scale hypoxic zones can persist for an extended period of time in the turbulent environment of a wave- and surge- exposed coral reef. This work highlights how the combination of three-dimensional imagery, biogenic fluxes, and fluid dynamic modeling can provide a powerful tool to illustrate and predict the distribution of analytes (e.g., oxygen or other bioactive substances) in a highly complex system. 

The rapidly advancing field of metabolomics encompasses a diverse suite of powerful analytical and bioinformatic tools that can help to reveal the diversity and activity of chemical compounds in individual organisms, species interactions, and entire ecosystems. In this perspective we use examples from studies of coral reefs to illustrate ways in which metabolomics has been and can be applied to understand coastal ecosystems. Examples of new insights that can be provided by metabolomics include resolving metabolite exchange between plants, animals and their microbiota, identifying the relevant metabolite exchanges associated with the onset and maintenance of diverse, microbial mutualisms characterizing unknown molecules that act as cues in coral, reproduction, or defining the suites of compounds involved in coral-algal competition and microbialization of algal-dominated ecosystems. Here we outline sampling, analytical and informatic methods that marine biologists and ecologists can apply to understand the role of chemical processes in ecosystems, with a focus on open access data analysis workflows and democratized databases. Finally, we demonstrate how these metabolomics tools and bioinformatics approaches can provide scientists the opportunity to map detailed metabolic inventories and dynamics for a holistic view of the relationships among reef organisms, their symbionts and their surrounding marine environment. 

Metabolites exuded by primary producers comprise a significant fraction of marine dissolved organic matter, a poorly characterized, heterogenous mixture that dictates microbial metabolism and biogeochemical cycling. We present a foundational untargeted molecular analysis of exudates released by coral reef primary producers using liquid chromatography–tandem mass spectrometry to examine compounds produced by two coral species and three types of algae (macroalgae, turfing microalgae, and crustose coralline algae [CCA]) from Mo’orea, French Polynesia. Of 10,568 distinct ion features recovered from reef and mesocosm waters, 1,667 were exuded by producers; the majority (86%) were organism specific, reflecting a clear divide between coral and algal exometabolomes. These data allowed us to examine two tenets of coral reef ecology at the molecular level. First, stoichiometric analyses show a significantly reduced nominal carbon oxidation state of algal exometabolites than coral exometabolites, illustrating one ecological mechanism by which algal phase shifts engender fundamental changes in the biogeochemistry of reef biomes. Second, coral and algal exometabolomes were differentially enriched in organic macronutrients, revealing a mechanism for reef nutrient-recycling. Coral exometabolomes were enriched in diverse sources of nitrogen and phosphorus, including tyrosine derivatives, oleoyl-taurines, and acyl carnitines. Exometabolites of CCA and turf algae were significantly enriched in nitrogen with distinct signals from polyketide macrolactams and alkaloids, respectively. Macroalgal exometabolomes were dominated by nonnitrogenous compounds, including diverse prenol lipids and steroids. This study provides molecular-level insights into biogeochemical cycling on coral reefs and illustrates how changing benthic cover on reefs influences reef water chemistry with implications for microbial metabolism.