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1. 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)

   Abstract 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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2. Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals

   https://doi.org/10.3390/microorganisms9091873  

   Messyasz, Adriana; Maher, Rebecca L.; Meiling, Sonora S.; Thurber, Rebecca Vega (September 2021, Microorganisms)

   null (Ed.)

   While studies show that nutrient pollution shifts reef trophic interactions between fish, macroalgae, and corals, we know less about how the microbiomes associated with these organisms react to such disturbances. To investigate how microbiome dynamics are affected during nutrient pollution, we exposed replicate Porites lobata corals colonized by the fish Stegastes nigricans, which farm an algal matrix on the coral, to a pulse of nutrient enrichment over a two-month period and examined the microbiome of each partner using 16S amplicon analysis. We found 51 amplicon sequence variants (ASVs) shared among the three hosts. Coral microbiomes had the lowest diversity with over 98% of the microbiome dominated by a single genus, Endozoicomonas. Fish and algal matrix microbiomes were ~20 to 70× more diverse and had higher evenness compared to the corals. The addition of nutrients significantly increased species richness and community variability between samples of coral microbiomes but not the fish or algal matrix microbiomes, demonstrating that coral microbiomes are less resistant to nutrient pollution than their trophic partners. Furthermore, the 51 common ASVs within the 3 hosts indicate microbes that may be shared or transmitted between these closely associated organisms, including Vibrionaceae bacteria, many of which can be pathogenic to corals. 

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3. Influence of reef habitat on coral microbial associations

   https://doi.org/10.1111/1758-2229.70051  

   Gantt, Shelby_E; Kemp, Keri_M; Colin, Patrick_L; Hoadley, Kenneth_D; LaJeunesse, Todd_C; Warner, Mark_E; Kemp, Dustin_W (November 2024, Environmental Microbiology Reports)

   Abstract Corals have complex symbiotic associations that can be influenced by the environment. We compare symbiotic dinoflagellate (family: Symbiodiniaceae) associations and the microbiome of five scleractinian coral species from three different reef habitats in Palau, Micronesia. Although pH and temperature corresponded with specific host‐Symbiodiniaceae associations common to the nearshore and offshore habitats, bacterial community dissimilarity analyses indicated minimal influence of these factors on microbial community membership for the coralsCoelastrea aspera,Psammocora digitata, andPachyseris rugosa. However, coral colonies sampled close to human development exhibited greater differences in microbial community diversity compared to the nearshore habitat for the coral speciesCoelastrea aspera,Montipora foliosa, andPocillopora acuta, and the offshore habitat forCoelastrea aspera, while also showing less consistency in Symbiodiniaceae associations. These findings indicate the influence that habitat location has on the bacterial and Symbiodiniaceae communities comprising the coral holobiont and provide important considerations for the conservation of coral reef communities, especially for island nations with increasing human populations and development. 

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4. 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)

   Summary 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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5. Systematic review of cnidarian microbiomes reveals insights into the structure, specificity, and fidelity of marine associations

   https://doi.org/10.1038/s41467-023-39876-6  

   McCauley, M.; Goulet, T. L.; Jackson, C. R.; Loesgen, S. (August 2023, Nature Communications)

   Abstract Microorganisms play essential roles in the health and resilience of cnidarians. Understanding the factors influencing cnidarian microbiomes requires cross study comparisons, yet the plethora of protocols used hampers dataset integration. We unify 16S rRNA gene sequences from cnidarian microbiome studies under a single analysis pipeline. We reprocess 12,010 cnidarian microbiome samples from 186 studies, alongside 3,388 poriferan, 370 seawater samples, and 245 cultured Symbiodiniaceae, unifying ~6.5 billion sequence reads. Samples are partitioned by hypervariable region and sequencing platform to reduce sequencing variability. This systematic review uncovers an incredible diversity of 86 archaeal and bacterial phyla associated with Cnidaria, and highlights key bacteria hosted across host sub-phylum, depth, and microhabitat. Shallow (< 30 m) water Alcyonacea and Actinaria are characterized by highly shared and relatively abundant microbial communities, unlike Scleractinia and most deeper cnidarians. Utilizing the V4 region, we find that cnidarian microbial composition, richness, diversity, and structure are primarily influenced by host phylogeny, sampling depth, and ocean body, followed by microhabitat and sampling date. We identify host and geographical generalist and specificEndozoicomonasclades within Cnidaria and Porifera. This systematic review forms a framework for understanding factors governing cnidarian microbiomes and creates a baseline for assessing stress associated dysbiosis. 

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