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1. Thermal Stress Interacts With Surgeonfish Feces to Increase Coral Susceptibility to Dysbiosis and Reduce Tissue Regeneration

   https://doi.org/10.3389/fmicb.2021.620458  

   Ezzat, Leïla ; Merolla, Sarah ; Clements, Cody S. ; Munsterman, Katrina S. ; Landfield, Kaitlyn ; Stensrud, Colton ; Schmeltzer, Emily R. ; Burkepile, Deron E. ; Vega Thurber, Rebecca ( March 2021 , Frontiers in Microbiology)

   null (Ed.)

   Dysbiosis of coral microbiomes results from various biotic and environmental stressors, including interactions with important reef fishes which may act as vectors of opportunistic microbes via deposition of fecal material. Additionally, elevated sea surface temperatures have direct effects on coral microbiomes by promoting growth and virulence of opportunists and putative pathogens, thereby altering host immunity and health. However, interactions between these biotic and abiotic factors have yet to be evaluated. Here, we used a factorial experiment to investigate the combined effects of fecal pellet deposition by the widely distributed surgeonfish Ctenochaetus striatus and elevated sea surface temperatures on microbiomes associated with the reef-building coral Porites lobata . Our results showed that regardless of temperature, exposure of P. lobata to C. striatus feces increased alpha diversity, dispersion, and lead to a shift in microbial community composition – all indicative of microbial dysbiosis. Although elevated temperature did not result in significant changes in alpha and beta diversity, we noted an increasing number of differentially abundant taxa in corals exposed to both feces and thermal stress within the first 48h of the experiment. These included opportunistic microbial lineages and taxa closely related to potential coral pathogens (i.e., Vibrio vulnificus , Photobacterium rosenbergii ). Some of these taxa were absent in controls but present in surgeonfish feces under both temperature regimes, suggesting mechanisms of microbial transmission and/or enrichment from fish feces to corals. Importantly, the impact to coral microbiomes by fish feces under higher temperatures appeared to inhibit wound healing in corals, as percentages of tissue recovery at the site of feces deposition were lower at 30°C compared to 26°C. Lower percentages of tissue recovery were associated with greater relative abundance of several bacterial lineages, with some of them found in surgeonfish feces (i.e., Rhodobacteraceae, Bdellovibrionaceae, Crocinitomicaceae). Our findings suggest that fish feces interact with elevated sea surface temperatures to favor microbial opportunism and enhance dysbiosis susceptibility in P. lobata . As the frequency and duration of thermal stress related events increase, the ability of coral microbiomes to recover from biotic stressors such as deposition of fish feces may be greatly affected, ultimately compromising coral health and resilience. 

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2. Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral‐associated microbes

   https://doi.org/10.1111/1758-2229.12686  

   Huggett, Megan J. ; Apprill, Amy ( September 2018 , Environmental Microbiology Reports)

   Coral‐associated microorganisms are thought to play a fundamental role in the health and ecology of corals, but understanding of specific coral–microbial interactions are lacking. In order to create a framework to examine coral–microbial specificity, we integrated and phylogenetically compared 21,100 SSU rRNA gene Sanger‐produced sequences from bacteria and archaea associated with corals from previous studies, and accompanying host, location and publication metadata, to produce the Coral Microbiome Database. From this database, we identified 39 described and candidate phyla of Bacteria and two Archaea phyla associated with corals, demonstrating that corals are one of the most phylogenetically diverse animal microbiomes. Secondly, this new phylogenetic resource shows that certain microorganisms are indeed specific to corals, including evolutionary distinct hosts. Specifically, we identified 2–37 putative monophyletic, coral‐specific sequence clusters within bacterial genera associated with the greatest number of coral species (Vibrio,EndozoicomonasandRuegeria) as well as functionally relevant microbial taxa (“CandidatusAmoebophilus”, “CandidatusNitrosopumilus” and under recognized cyanobacteria). This phylogenetic resource provides a framework for more targeted studies of corals and their specific microbial associates, which is timely given the escalated need to understand the role of the coral microbiome and its adaptability to changing ocean and reef conditions.

    

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3. Structure and stability of the coral microbiome in space and time

   https://doi.org/10.1038/s41598-019-43268-6  

   Dunphy, Courtney M. ; Gouhier, Tarik C. ; Chu, Nathaniel D. ; Vollmer, Steven V. ( May 2019 , Scientific Reports)

   Although it is well established that the microbial communities inhabiting corals perform key functions that promote the health and persistence of their hosts, little is known about their spatial structure and temporal stability. We examined the natural variability of microbial communities associated with six Caribbean coral species from three genera at four reef sites over one year. We identified differences in microbial community composition between coral genera and species that persisted across space and time, suggesting that local host identity likely plays a dominant role in structuring the microbiome. However, we found that microbial community dissimilarity increased with geographical distance, which indicates that regional processes such as dispersal limitation and spatiotemporal environmental heterogeneity also influence microbial community composition. In addition, network analysis revealed that the strength of host identity varied across coral host genera, with species from the genusAcroporahaving the most influence over their microbial community. Overall, our results demonstrate that despite high levels of microbial diversity, coral species are characterized by signature microbiomes that are stable in both space and time.

    

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4. Shifts in the coral microbiome in response to in situ experimental deoxygenation

   https://doi.org/10.1128/aem.00577-23  

   Howard, Rachel D. ; Schul, Monica D. ; Rodriguez Bravo, Lucia M. ; Altieri, Andrew H. ; Meyer, Julie L. ( November 2023 , Applied and Environmental Microbiology)

   Biddle, Jennifer F. (Ed.)

   Global climate change impacts marine ecosystems through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, less is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their tolerance to hypoxia. We conductedin situoxygen manipulations on a coral reef in Bahía Almirante on the Caribbean coast of Panama, which has previously experienced documented episodes of hypoxia. Naïve coral colonies (previously unexposed to hypoxia) ofSiderastrea sidereaandAgaricia lamarckiwere transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress or may represent opportunists exploiting host stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor.

   Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels aroundSiderastrea sidereaandAgaricia lamarckicoloniesin situto observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress.

    

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5. Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

   https://doi.org/10.1111/gcb.17088  

   Vompe, Alex D. ; Epstein, Hannah E. ; Speare, Kelly E. ; Schmeltzer, Emily R. ; Adam, Thomas C. ; Burkepile, Deron E. ; Sharpton, Thomas J. ; Vega Thurber, Rebecca ( December 2023 , Global Change Biology)

   Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large‐scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long‐term (28 months, 2018–2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves inAcropora retusa,Porites lobata, andPocilloporaspp., which included: microbiome acclimatization inA. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocilloporaspp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusaboth significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobatacolonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality inA. retusa. This study reveals evidence for coral species‐specific microbial responses to repeated heatwaves and, importantly, suggests that host‐dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.

    

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