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ABSTRACT Benthic–pelagic coupling, the reciprocal exchange of materials between benthic and pelagic habitats, has traditionally emphasised pelagic influences on benthic systems. Yet, the role of benthic biological processes in shaping pelagic microbial dynamics remains underexplored. We investigated how surfgrass and mussels regulate nitrogen and dissolved organic matter (DOM) cycling and their cascading effects on heterotrophic bacteria in Oregon tide pools. We quantified biogeochemical fluxes and bacterial responses before and after foundation species removal during contrasting upwelling regimes. Mussel‐dominated pools released high concentrations of ammonium and nitrate, while surfgrass pools transformed DOM that fueled bacterial growth; upwelling intensified these benthic–pelagic linkages. Removing foundation species dampened nutrient release in mussel pools and reduced DOM‐fueled bacterial growth in surfgrass pools, ultimately decoupling benthic productivity from pelagic microbial growth. Our results demonstrate the critical role of foundation species to pelagic microbial processes and underscore the vulnerability of coastal microbial dynamics to their global decline. 

Abstract The existence of highly productive coral reefs within oligotrophic gyres is in part due to intensive recycling of macronutrients and organic matter by microbes. Therefore, characterizing reef bacterioplankton communities is key for understanding reef metabolism and biogeochemical transformations. We performed a high‐resolution survey of waters surrounding Mo'orea (French Polynesia), coupling 16S metabarcoding with biogeochemical and physical measurements. Bacterioplankton communities differed markedly among reef ecosystems on three sides of the island, and within each system distinct communities emerged in forereef, backreef and reef pass habitats. The degree of habitat differentiation varied among the island sides according to current speeds inferred from wave power. Oceanic‐associated taxa were enriched in forereefs and throughout western reefs with highest wave power and lowest productivity. Reef‐associated taxa were enriched in backreef and pass habitats most strongly on northern reefs with lowest wave power and highest productivity. Our results offer insight into dynamics regulating reef microbial communities. 

Abstract Nutrient availability drives community structure and ecosystem processes, especially in tropical lagoons that are typically oligotrophic but often receive allochthonous inputs from land. Terrestrially derived nutrients are introduced to tropical lagoons by surface runoff and submarine groundwater discharge, which are influenced by seasonal precipitation. However, terrigenous inputs presumably diminish along the onshore–offshore gradients within lagoons. We characterized nutrient availability in the lagoons of a tropical high island, Moorea, French Polynesia, using spatially distributed measurements of nitrogen content in the tissues of a widespread macroalga during the rainy season over 4 yr. We used synoptic water column sampling to identify associations among macroalgal nutrient content and the composition of inorganic macronutrients, dissolved organic matter, and microbial communities. We paired these data with quantifications of land use in nearby watersheds to uncover links between terrestrial factors, aquatic chemistry, and microbial communities. Algal N content was highest near shore and near large, human‐impacted watersheds, and lower at offshore sites. Sites with high algal N had water columns with high nitrite + nitrate, silicate, and increased humic organic matter (based on a fluorescence Humification Index), especially following rain. Microbial communities were differentiated among nearshore habitats and covaried with algal N and water chemistry, supporting the hypothesis that terrigenous nutrient enrichment shapes microbial dynamics in otherwise oligotrophic tropical lagoons. This study reveals that land–sea connections create nutrient subsidies that are important for lagoon biogeochemistry and microbiology, indicating that future changes in land use or precipitation will modify ecosystem processes in tropical lagoons. 

Abstract Islands in oligotrophic oceans act as local sources of nutrients. These nutrients originate from land and from deep oceanic nutrients introduced to the photic zone by tides, currents, and internal waves interacting with island bathymetry. These processes create the island mass effect (IME), in which increased chlorophylla(Chla) is found near islands compared to oceanic waters. The IME has been described via satellite observations, but the effects on phytoplankton community structure are not well documented. From 2013 to 2020, chlorophyll, nutrient, and picoplankton samples were collected from multiple depths on quarterly cruises at two sites south of O'ahu, Hawai'i.Prochlorococcus,Synechococcus, picoeukaryotes, and heterotrophic bacteria were enumerated using flow cytometry. We compared nearshore results to Sta. ALOHA, 100 km from O'ahu. Consistent with the expected IME, Chlaconcentrations were significantly enhanced at both nearshore sites compared to Sta. ALOHA.Prochlorococcusconcentrations increased with greater distance from shore, particularly below 50 m; mixed layer concentrations ofSynechococcusand picoeukaryotes significantly decreased with greater distance from shore, as did concentrations of nitrate and phosphate below the mixed layer. Heterotrophic bacteria concentrations did not show a spatial trend. Carbon‐based biomass estimates of the picoplankton population indicated that the IME‐associated Chlaincreases near the island are likely driven by larger phytoplankton classes. This study describes the IME‐associated shift in the picophytoplankton community distribution, which has implications for nutrient cycling, food web dynamics and fisheries in oligotrophic island ecosystems, and adds to the understanding of spatial heterogeneity in carbon fixation in the ocean. 

ABSTRACT Dissolved organic matter (DOM) comprises diverse compounds with variable bioavailability across aquatic ecosystems. The sources and quantities of DOM can influence microbial growth and community structure with effects on biogeochemical processes. To investigate the chemodiversity of labile DOM in tropical reef waters, we tracked microbial utilisation of over 3000 untargeted mass spectrometry ion features exuded from two coral and three algal species. Roughly half of these features clustered into over 500 biologically labile spectral subnetworks annotated to diverse structural superclasses, including benzenoids, lipids, organic acids, heterocyclics and phenylpropanoids, comprising on average one‐third of the ion richness and abundance within each chemical class. Distinct subsets of these labile compounds were exuded by algae and corals during the day and night, driving differential microbial growth and substrate utilisation. This study expands the chemical diversity of labile marine DOM with implications for carbon cycling in coastal environments. 

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. 

Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce genomic information about the microbiota that perform this degradation. This study explores the potential ofKyphosusgastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae throughin silicostudy of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously describedKyphosusgut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa inKyphosusguts. The most versatile of the recovered MAGs were from theBacteroidotaphylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from theBacillota(genusVallitalea) andVerrucomicrobiota(orderKiritimatiellales) highlight the importance of metabolic contributions from multiple phyla to broaden polysaccharide degradation capabilities. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level amongKyphosussymbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors.IMPORTANCESeaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genusKyphosusfeed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study reconstructs metagenome-assembled genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identifyKyphosusguts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides. 

Abstract The dominant benthic primary producers in coral reef ecosystems are complex holobionts with diverse microbiomes and metabolomes. In this study, we characterize the tissue metabolomes and microbiomes of corals, macroalgae, and crustose coralline algae via an intensive, replicated synoptic survey of a single coral reef system (Waimea Bay, Oʻahu, Hawaii) and use these results to define associations between microbial taxa and metabolites specific to different hosts. Our results quantify and constrain the degree of host specificity of tissue metabolomes and microbiomes at both phylum and genus level. Both microbiome and metabolomes were distinct between calcifiers (corals and CCA) and erect macroalgae. Moreover, our multi-omics investigations highlight common lipid-based immune response pathways across host organisms. In addition, we observed strong covariation among several specific microbial taxa and metabolite classes, suggesting new metabolic roles of symbiosis to further explore. 

The addition of terrestrial inputs to the ocean can have cascading impacts on coastal biogeochemistry by directly altering the water chemistry and indirectly changing ecosystem metabolism, which also influences water chemistry. Here, we use submarine groundwater discharge (SGD) as a model system to examine the direct geochemical and indirect biologically mediated effects of terrestrial nutrient subsidies on a fringing coral reef. We hypothesize that the addition of new solutes from SGD alters ecosystem metabolic processes including net ecosystem production and calcification, thereby changing the patterns of uptake and release of carbon by benthic organisms. SGD is a common land–sea connection that delivers terrestrially sourced nutrients, carbon dioxide, and organic matter to coastal ecosystems. Our research was conducted at two distinct coral reefs in Moʻorea, French Polynesia, characterized by contrasting flow regimes and SGD biogeochemistry. Using a Bayesian structural equation model, our research elucidates the direct geochemical and indirect biologically mediated effects of SGD on both dissolved organic and inorganic carbon pools. We reveal that SGD‐derived nutrients enhance both net ecosystem production and respiration. Furthermore, the study demonstrates that SGD‐induced alterations in net ecosystem production significantly influence pH dynamics, ultimately impacting net ecosystem calcification. Notably, the study underscores the context‐dependent nature of these cascading direct and indirect effects resulting from SGD, with flow conditions and the composition of the terrestrial inputs playing pivotal roles. Our research provides valuable insights into the interplay between terrestrial inputs and coral reef ecosystems, advancing our understanding of coastal carbon cycling and the broader implications of allochthonous inputs on ecosystem functioning.