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1. Coral high molecular weight carbohydrates support opportunistic microbes in bacterioplankton from an algae-dominated reef

   https://doi.org/10.1128/msystems.00832-24  

   Thobor, Bianca M; Haas, Andreas F; Wild, Christian; Nelson, Craig E; Wegley_Kelly, Linda; Hehemann, Jan-Hendrik; Arts, Milou; Boer, Meine; Buck-Wiese, Hagen; Nguyen, Nguyen P; et al (November 2024, mSystems)

   Meyer, Julie L (Ed.)

   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. 

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2. Coral reef biofilm bacterial diversity and successional trajectories are structured by reef benthic organisms and shift under chronic nutrient enrichment

   https://doi.org/10.1038/s41522-021-00252-1  

   Remple, Kristina L.; Silbiger, Nyssa J.; Quinlan, Zachary A.; Fox, Michael D.; Kelly, Linda Wegley; Donahue, Megan J.; Nelson, Craig E. (December 2021, npj Biofilms and Microbiomes)

   Abstract Work on marine biofilms has primarily focused on host-associated habitats for their roles in larval recruitment and disease dynamics; little is known about the factors regulating the composition of reef environmental biofilms. To contrast the roles of succession, benthic communities and nutrients in structuring marine biofilms, we surveyed bacteria communities in biofilms through a six-week succession in aquaria containing macroalgae, coral, or reef sand factorially crossed with three levels of continuous nutrient enrichment. Our findings demonstrate how biofilm successional trajectories diverge from temporal dynamics of the bacterioplankton and how biofilms are structured by the surrounding benthic organisms and nutrient enrichment. We identify a suite of biofilm-associated bacteria linked with the orthogonal influences of corals, algae and nutrients and distinct from the overlying water. Our results provide a comprehensive characterization of marine biofilm successional dynamics and contextualize the impact of widespread changes in reef community composition and nutrient pollution on biofilm community structure. 

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3. Submarine groundwater discharge drives both direct and indirect effects on organismal and community metabolism on coral reefs

   https://doi.org/10.1098/rspb.2024.1554  

   Barnas, Danielle M; Zeff, Maya; Silbiger, Nyssa J (January 2025, Proceedings of the Royal Society B: Biological Sciences)

   Coral reefs experience numerous environmental gradients affecting organismal physiology and species biodiversity, which ultimately impact community metabolism. This study shows that submarine groundwater discharge (SGD), a common natural environmental gradient in coastal ecosystems associated with decreasing temperatures, salinity and pH with increasing nutrients, has both direct and indirect effects on coral reef community metabolism by altering individual growth rates and community composition. Our data revealed that SGD exposure hindered the growth of two algae,Halimeda opuntiaandValonia fastigiata,by 67 and 200%, respectively, and one coral,Porites rus,by 20%. Community metabolic rates showed altered community production, respiration and calcification between naturally high and low exposure areas mostly due to differences in community identity (i.e. species composition), rather than a direct effect of SGD on physiology. Production and calcification were 1.5 and 6.5 times lower in assemblages representing high SGD communities regardless of environment. However, the compounding effect of community identity and SGD exposure on respiration resulted in the low SGD community exhibiting the highest respiration rates under higher SGD exposure. By demonstrating SGD’s role in altering community composition and metabolism, this research highlights the critical need to consider compounding environmental gradients (i.e. nutrients, salinity and temperature) in the broader context of ecosystem functions. 

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4. Linking photoacclimation responses and microbiome shifts between depth-segregated sibling species of reef corals

   https://doi.org/10.1098/rsos.211591  

   Prada, Carlos; López-Londoño, Tomás; Pollock, F. Joseph; Roitman, Sofia; Ritchie, Kim B.; Levitan, Don R.; Knowlton, Nancy; Woodley, Cheryl; Iglesias-Prieto, Roberto; Medina, Mónica (March 2022, Royal Society Open Science)

   Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the corals Orbicella annularis and O. franksi , two young species with contrasting vertical distribution in the Caribbean. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation and low mortality, and maintained a consistent bacterial community. By contrast, O. annularis experienced high mortality and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts. 

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5. Distinguishing the molecular diversity, nutrient content, and energetic potential of exometabolomes produced by macroalgae and reef-building corals

   https://doi.org/10.1073/pnas.2110283119  

   Wegley_Kelly, Linda; Nelson, Craig E.; Petras, Daniel; Koester, Irina; Quinlan, Zachary A.; Arts, Milou G.I.; Nothias, Louis-Felix; Comstock, Jacqueline; White, Brandie M.; Hopmans, Ellen C.; et al (February 2022, Proceedings of the National Academy of Sciences)

   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. 

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