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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 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 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. 

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. 

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. 

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,Montipora capitataandPorites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressaexhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitatarepeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitatadisplayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressaappeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene. 

Submarine groundwater discharge (SGD) in high volcanic islands can be an important source of freshwater and nutrients to coral reefs. High inorganic nutrient content is generally thought to augment primary production in coastal systems but when this is delivered via a freshwater vector as is the case with SGD in this study, the effects on productivity are unclear. In the current literature, there is limited evidence for a direct association between SGD and primary productivity of reefs. To elucidate the response of primary productivity to SGD, we conducted spatially and temporally explicit in situ benthic chamber experiments on a reef flat along a gradient of SGD. We found significant quadratic relationships between C-uptake and SGD for both phytoplankton and the most abundant macroalga, Gracilaria salicornia , with uptake maxima at SGD-derived salinities of ~21−22 (24.5−26.6 μmol NO 3 -L −1 ). These results suggest a physiological tradeoff between salinity tolerance and nutrient availability for reef primary producers. Spatially explicit modeling of reefs with SGD and without SGD indicate reef-scale G. salicornia and phytoplankton C-uptake decreased by 82% and 36% in the absence of SGD, respectively. Thus, nutrient-rich and low salinity SGD has significant effects on algal C-uptake in reef systems. 

To thrive in nutrient-poor waters, coral reefs must retain and recycle materials efficiently. This review centers microbial processes in facilitating the persistence and stability of coral reefs, specifically the role of these processes in transforming and recycling the dissolved organic matter (DOM) that acts as an invisible currency in reef production, nutrient exchange, and organismal interactions. The defining characteristics of coral reefs, including high productivity, balanced metabolism, high biodiversity, nutrient retention, and structural complexity, are inextricably linked to microbial processing of DOM. The composition of microbes and DOM in reefs is summarized, and the spatial and temporal dynamics of biogeochemical processes carried out by microorganisms in diverse reef habitats are explored in a variety of key reef processes, including decomposition, accretion, trophictransfer, and macronutrient recycling. Finally, we examine how widespread habitat degradation of reefs is altering these important microbe–DOM interactions, creating feedbacks that reduce reef resilience to global change.