The coral microbiome in sickness, in health and in a changing world

Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505 (2015).

Article  CAS  PubMed  Google Scholar 

Knowlton, N. et al. Rebuilding coral reefs: a decadal grand challenge (International Coral Reef Society and Future Earth Coasts, 2021).

Eddy, T. D. et al. Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4, 1278–1285 (2021).

Article  ADS  Google Scholar 

Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).

Article  CAS  PubMed  Google Scholar 

Pogoreutz, C. et al. in Cellular Dialogues in the Holobiont (eds Bosch, T. C. G. & Hadfield, M. G.) 91–118 (CRC, 2020).

Rohwer, F., Seguritan, V. & Azam, F. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 85, 37–48 (2002).

Google Scholar 

Jaspers, C. et al. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. Zoology 133, 81–87 (2019).

Article  PubMed  Google Scholar 

LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580.e6 (2018).

Article  CAS  PubMed  Google Scholar 

Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl Acad. Sci. USA 118, e2022653118 (2021).

Article  PubMed  PubMed Central  Google Scholar 

van Oppen, M. J. H. & Blackall, L. L. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17, 557–567 (2019).

Article  PubMed  Google Scholar 

Thurber, R. V., Payet, J. P., Thurber, A. R. & Correa, A. M. S. Virus–host interactions and their roles in coral reef health and disease. Nat. Rev. Microbiol. 15, 205–216 (2017).

Article  CAS  PubMed  Google Scholar 

Bonacolta, A. M. et al. Beyond the Symbiodiniaceae: diversity and role of microeukaryotic coral symbionts. Coral Reefs 42, 567–577 (2023).

Article  Google Scholar 

Peixoto, R. S. et al. Harnessing the microbiome to prevent global biodiversity loss. Nat. Microbiol. 7, 1–10 (2022).

Article  Google Scholar 

Voolstra, C. R. et al. Extending the natural adaptive capacity of coral holobionts. Nat. Rev. Earth Environ. 2, 747–762 (2021).

Article  ADS  Google Scholar 

Ziegler, M. et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 3092 (2019).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Voolstra, C. R. & Ziegler, M. Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. Bioessays 42, e2000004 (2020).

Article  PubMed  Google Scholar 

Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Santoro, E. P. et al. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci. Adv. 7, eabg3088 (2021).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Matthews, J. L. et al. Symbiodiniaceae–bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks. Environ. Microbiol. 22, 1675–1687 (2020).

Article  PubMed  Google Scholar 

Schultz, J. et al. Methods and strategies to uncover coral-associated microbial dark matter. mSystems 7, e0036722 (2022).

Article  PubMed  Google Scholar 

Sweet, M. et al. Insights into the cultured bacterial fraction of corals. mSystems 6, e0124920 (2021).

Article  PubMed  Google Scholar 

Pogoreutz, C. et al. Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle. ISME J. 16, 1883–1895 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cárdenas, A. et al. Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility. ISME J. 16, 2406–2420 (2022).

Article  PubMed  PubMed Central  Google Scholar 

Robbins, S. J. et al. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat. Microbiol. 4, 2090–2100 (2019).

Article  PubMed  Google Scholar 

Hochart, C. et al. Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean. Nat. Commun. 14, 3037 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Dörr, M. et al. Short-term heat stress assays resolve effects of host strain, repeat stress, and bacterial inoculation on Aiptasia thermal tolerance phenotypes. Coral Reefs 42, 1–11 (2023).

Article  Google Scholar 

Pollock, F. J. et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9, 4921 (2018).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Buitrago-López, C. et al. Disparate population and holobiont structure of pocilloporid corals across the Red Sea gradient demonstrate species-specific evolutionary trajectories. Mol. Ecol. 32, 2151–2173 (2023).

Article  PubMed  Google Scholar 

Rädecker, N. et al. Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling. ISME J. 16, 1110–1118 (2021).

Article  PubMed  PubMed Central  Google Scholar 

Chan, W. Y., Rudd, D. & van Oppen, M. J. Spatial metabolomics for symbiotic marine invertebrates. Life Sci. Alliance 6, e202301900 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Peixoto, R. S. et al. Coral probiotics: premise, promise, prospects. Annu. Rev. Anim. Biosci. 9, 265–288 (2021).

Article  PubMed  Google Scholar 

van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl Acad. Sci. USA 112, 2307–2313 (2015).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073 (2006).

Article  CAS  PubMed  Google Scholar 

O’Brien, P. A. et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 14, 2211–2222 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 11, 186–200 (2017).

Article  PubMed  Google Scholar 

Roder, C., Bayer, T., Aranda, M., Kruse, M. & Voolstra, C. R. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol. Ecol. 24, 3501–3511 (2015).

Article  PubMed  PubMed Central  Google Scholar 

Chan, W. Y., Peplow, L. M., Menéndez, P., Hoffmann, A. A. & van Oppen, M. J. H. The roles of age, parentage and environment on bacterial and algal endosymbiont communities in Acropora corals. Mol. Ecol. 28, 3830–3843 (2019).

Article  CAS  PubMed  Google Scholar 

Rosenberg, Y. et al. Urbanization comprehensively impairs biological rhythms in coral holobionts. Glob. Chang. Biol. 28, 3349–3364 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Röthig, T., Roik, A., Yum, L. K. & Voolstra, C. R. Distinct bacterial microbiomes associate with the deep-sea coral Eguchipsammia fistula from the Red Sea and from aquaria settings. Front. Mar. Sci. 4, 259 (2017).

Article  Google Scholar 

Hadaidi, G. et al. Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas. Sci. Rep. 7, 45362 (2017).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Pogoreutz, C. et al. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8, 2240–2252 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Haydon, T. D. et al. Rapid shifts in bacterial communities and homogeneity of symbiodiniaceae in colonies of Pocillopora acuta transplanted between reef and mangrove environments. Front. Microbiol. 12, 756091 (2021).

Article  PubMed  PubMed Central  Google Scholar 

Damjanovic, K., Menéndez, P., Blackall, L. L. & van Oppen, M. J. H. Mixed-mode bacterial transmission in the common brooding coral Pocillopora acuta. Environ. Microbiol. 22, 397–412 (2020).

Article  CAS  PubMed  Google Scholar 

Sharp, K. H., Ritchie, K. B., Schupp, P. J., Ritson-Williams, R. & Paul, V. J. Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS ONE 5, e10898 (2010).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Damjanovic, K., Blackall, L. L., Menéndez, P. & van Oppen, M. J. H. Bacterial and algal symbiont dynamics in early recruits exposed to two adult coral species. Coral Reefs 39, 189–202 (2020).

Article  Google Scholar 

Dubé, C. E. et al. Naturally occurring fire coral clones demonstrate a genetic and environmental basis of microbiome composition. Nat. Commun. 12, 6402 (2021).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Strader, M. E. et al. Nitrate enrichment has lineage specific effects on Pocillopora acuta adults, but no transgenerational effects in planulae. Coral Reefs 41, 303–317 (2022).

Article  Google Scholar 

Luo, D. et al. Population differentiation of Rhodobacteraceae along with coral compartments. ISME J. 15, 3286–3302 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Huggett, M. J. & Apprill, A. Coral microbiome database: integration of sequences reveals high diversity and relatedness of coral-associated microbes. Environ. Microbiol. Rep. 11, 372–385 (2019).

Article  PubMed  Google Scholar 

Oren, A. & Garrity, G. M. Valid publication of the names of forty-two phyla of prokaryotes. Int. J. Syst. Evol. Microbiol. 71, 005056 (2021).

Article  Google Scholar 

Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

Article  CAS  PubMed  Google Scholar 

Mohamed, A. R., Ochsenkühn, M. A., Kazlak, A. M., Moustafa, A. & Amin, S. A. The coral microbiome: towards an understanding of the molecular mechanisms of coral–microbiota interactions. FEMS Microbiol. Rev. 47, fuad005 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Galand, P. E. et al. Diversity of the Pacific Ocean coral reef microbiome. Nat. Commun. 14, 3039 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, C. R. Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci. Rep. 7, 40579 (2017).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Tandon, K. et al. Comparative genomics: dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP). ISME J. 14, 1290–1303 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324 (2016).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ide, K. et al. Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral. Microbiome 10, 220 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Voolstra, C. R. et al. Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance. Mol. Ecol. 30, 4466–4480 (2021).

Article  CAS  PubMed  Google Scholar 

Raina, J.-B., Tapiolas, D., Willis, B. L. & Bourne, D. G. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 75, 3492–3501 (2009).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Nissimov, J., Rosenberg, E. & Munn, C. B. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol. Lett. 292, 210–215 (2009).

Article  CAS  PubMed  Google Scholar 

Rosado, P. M. et al. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13, 921–936 (2019).

Article  CAS  PubMed  Google Scholar 

Rubio-Portillo, E., Ramos-Esplá, A. A. & Antón, J. Shifts in marine invertebrate bacterial assemblages associated with tissue necrosis during a heat wave. Coral Reefs 40, 395–404 (2021).

Article  Google Scholar 

Kitamura, R. et al. Specific detection of coral-associated ruegeria, a potential probiotic bacterium, in corals and subtropical seawater. Mar. Biotechnol. 23, 576–589 (2021).

Article  CAS  Google Scholar 

Levy, S. et al. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity. Cell 184, 2973–2987.e18 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hughes, D. J., Raina, J.-B., Nielsen, D. A., Suggett, D. J. & Kühl, M. Disentangling compartment functions in sessile marine invertebrates. Trends Ecol. Evol. 37, 740–748 (2022).

Article  PubMed  Google Scholar 

Pernice, M. et al. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J. 14, 325–334 (2020).

Article  PubMed  Google Scholar 

Sweet, M. J., Croquer, A. & Bythell, J. C. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30, 39–52 (2011).

Article  ADS  Google Scholar 

Ainsworth, T. D., Krause, L., Bridge, T. & Torda, G. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261–2274 (2015).

Article  CAS  Google Scholar 

Apprill, A., Weber, L. G. & Santoro, A. E. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems 1, e00143–e00216 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Marcelino, V. R., van Oppen, M. J. & Verbruggen, H. Highly structured prokaryote communities exist within the skeleton of coral colonies. ISME J. 12, 300–303 (2018).

Article  PubMed  Google Scholar 

Maire, J. et al. Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs. ISME J. 15, 2028–2042 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Maire, J. et al. Colocalization and potential interactions of Endozoicomonas and chlamydiae in microbial aggregates of the coral Pocillopora acuta. Sci. Adv. 9, eadg0773 (2023).

Article  CAS  PubMed  Google Scholar 

van Oppen, M. J. H. & Raina, J.-B. Coral holobiont research needs spatial analyses at the microbial scale. Environ. Microbiol. 25, 179–183 (2023).

Article  PubMed  Google Scholar 

Apprill, A. et al. Toward a new era of coral reef monitoring. Environ. Sci. Technol. 57, 5117–5124 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Schmidt, T. S. B., Matias Rodrigues, J. F. & von Mering, C. Ecological consistency of SSU rRNA-based operational taxonomic units at a global scale. PLoS Comput. Biol. 10, e1003594 (2014).

Article  PubMed  PubMed Central  Google Scholar 

Camp, E. F. et al. Micronutrient content drives elementome variability amongst the Symbiodiniaceae. BMC Plant. Biol. 22, 184 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pettay, D. T., Wham, D. C., Smith, R. T., Iglesias-Prieto, R. & LaJeunesse, T. C. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc. Natl Acad. Sci. USA 112, 7513–7518 (2015).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Vasquez Kuntz, K. L. et al. Inheritance of somatic mutations by animal offspring. Sci. Adv. 8, eabn0707 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kwong, W. K., Del Campo, J., Mathur, V., Vermeij, M. J. A. & Keeling, P. J. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568, 103–107 (2019).

Article  ADS  CAS  PubMed  Google Scholar 

Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 23, 490–497 (2015).

Article  PubMed  Google Scholar 

Hume, B. C. C., Mejia-Restrepo, A., Voolstra, C. R. & Berumen, M. L. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 39, 583–601 (2020).

Article  Google Scholar 

Dubé, C. E. et al. Algal symbioses with fire corals demonstrate host genotype specificity and niche adaptation at subspecies resolution. Preprint at bioRxiv https://doi.org/10.1101/2023.04.03.535406 (2023).

Burriesci, M. S., Raab, T. K. & Pringle, J. R. Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. J. Exp. Biol. 215, 3467–3477 (2012).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Rädecker, N., Escrig, S., Spangenberg, J. E., Voolstra, C. R. & Meibom, A. Coupled carbon and nitrogen cycling regulates the cnidarian-algal symbiosis. Nat. Commun. 14, 6948 (2023).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Ngugi, D. K., Ziegler, M., Duarte, C. M. & Voolstra, C. R. Genomic blueprint of glycine betaine metabolism in coral metaorganisms and their contribution to reef nitrogen budgets. iScience 23, 101120 (2020).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Del Campo, J., Pombert, J.-F., Šlapeta, J., Larkum, A. & Keeling, P. J. The ‘other’ coral symbiont: Ostreobium diversity and distribution. ISME J. 11, 296–299 (2017).

Article  PubMed  Google Scholar 

Fine, M. & Loya, Y. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. Biol. Sci. 269, 1205–1210 (2002).

Article  PubMed  PubMed Central  Google Scholar 

Janouškovec, J., Horák, A., Barott, K. L., Rohwer, F. L. & Keeling, P. J. Environmental distribution of coral-associated relatives of apicomplexan parasites. ISME J. 7, 444–447 (2013).

Article  PubMed  Google Scholar 

Mohamed, A. R. et al. Deciphering the nature of the coral–Chromera association. ISME J. 12, 776–790 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Lesser, M. P., Mazel, C. H., Gorbunov, M. Y. & Falkowski, P. G. Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305, 997–1000 (2004).

Article  ADS  CAS  PubMed  Google Scholar 

Yang, S.-H. et al. Metagenomic, phylogenetic, and functional characterization of predominant endolithic green sulfur bacteria in the coral Isopora palifera. Microbiome 7, 3 (2019).

Article  PubMed  PubMed Central  Google Scholar 

Tandon, K. et al. Genomic view of the diversity and functional role of archaea and bacteria in the skeleton of the reef-building corals Porites lutea and Isopora palifera. Gigascience 12, giac127 (2022).

Article  PubMed  Google Scholar 

Howe-Kerr, L. I. et al. Viruses of a key coral symbiont exhibit temperature-driven productivity across a reefscape. ISME Commun. 3, 27 (2023).

Article  PubMed  PubMed Central  Google Scholar 

Grupstra, C. G. B. et al. Thermal stress triggers productive viral infection of a key coral reef symbiont. ISME J. 16, 1430–1441 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cárdenas, A. et al. Coral-associated viral assemblages from the central Red Sea align with host species and contribute to holobiont genetic diversity. Front. Microbiol. 11, 572534 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Marhaver, K. L., Edwards, R. A. & Rohwer, F. Viral communities associated with healthy and bleaching corals. Environ. Microbiol. 10, 2277–2286 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

de Goeij, J. M. & van Duyl, F. C. Coral cavities are sinks of dissolved organic carbon (DOC). Limnol. Oceanogr. 52, 2608–2617 (2007).

Article  ADS  Google Scholar 

Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. Camb. Philos. Soc. 84, 1–17 (2009).

Article  PubMed  Google Scholar 

Pogoreutz, C. et al. Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching. Glob. Chang. Biol. 23, 3838–3848 (2017).

Article  ADS  PubMed  Google Scholar 

Haas, A. F. et al. Global microbialization of coral reefs. Nat. Microbiol. 1, 16042 (2016).

Article  CAS  PubMed  Google Scholar 

Nelson, C. E. et al. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 7, 962–979 (2013).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cárdenas, A. et al. Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton. ISME J. 12, 59–76 (2018).

Article  PubMed  Google Scholar 

Cui, G. et al. Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia. Sci. Adv. 9, eadf7108 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lesser, M. P. et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346, 143–152 (2007).

Article  ADS  CAS  Google Scholar 

Pogoreutz, C. et al. Nitrogen fixation aligns with nifH abundance and expression in two coral trophic functional groups. Front. Microbiol. 8, 1187 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Geissler, L. et al. Highly variable and non-complex diazotroph communities in corals from ambient and high CO2 environments. Front. Mar. Sci. 8, 754682 (2021).

Article  Google Scholar 

Bednarz, V. N., Grover, R., Maguer, J. F., Fine, M. & Ferrier-Pagès, C. The assimilation of diazotroph-derived nitrogen by scleractinian corals depends on their metabolic status. mBio 8, e02058-16 (2017).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Santos, H. F. et al. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. 8, 2272–2279 (2014).

Article  PubMed  PubMed Central  Google Scholar 

Wafar, M. M., Wafar, S. & David, J. J. Nitrification in reef corals. Limnol. Oceanogr. 35, 725–730 (1990).

Article  ADS  CAS  Google Scholar 

Tilstra, A. et al. Denitrification aligns with N2 fixation in Red Sea corals. Sci. Rep. 9, 19460 (2019).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Tilstra, A. et al. Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability. R. Soc. Open Sci. 8, 201835 (2021).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

El-Khaled, Y. C. et al. In situ eutrophication stimulates dinitrogen fixation, denitrification, and productivity in Red Sea coral reefs. Mar. Ecol. Prog. Ser. 645, 55–66 (2020).

Article  ADS  CAS  Google Scholar 

Gardner, S. G. G. et al. Increased DMSP availability during thermal stress influences DMSP-degrading bacteria in coral mucus. Front. Mar. Sci. 9, 912862 (2022).

Article  Google Scholar 

Curson, A. R. J., Todd, J. D., Sullivan, M. J. & Johnston, A. W. B. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 9, 849–859 (2011).

Article  CAS  PubMed  Google Scholar 

Kuek, F. W. I. et al. DMSP production by coral-associated bacteria. Front. Mar. Sci. 9, 869574 (2022).

Article  Google Scholar 

Frade, P. R. et al. Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus. Environ. Chem. 13, 252–265 (2015).

Article  Google Scholar 

Peixoto, R. S. et al. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 1–16 (2017).

Article  CAS  Google Scholar 

Yuen, Y. S., Yamazaki, S. S., Baird, A. H., Nakamura, T. & Yamasaki, H. Sulfate-reducing bacteria in the skeleton of the massive coral Goniastrea aspera from the great barrier reef. Galaxea J. Coral Reef Stud. 15, 154–159 (2013).

Article  Google Scholar 

Agostini, S. et al. Coral symbiotic complex: hypothesis through vitamin B12 for a new evaluation. Galaxea J. Coral Reef Stud. 11, 1–11 (2009).

Article  Google Scholar 

Li, J. et al. Cultured bacteria provide insight into the functional potential of the coral-associated microbiome. mSystems 7, e0032722 (2022).

Article  PubMed  Google Scholar 

Bernal, P., Llamas, M. A. & Filloux, A. Type VI secretion systems in plant-associated bacteria. Environ. Microbiol. 20, 1–15 (2018).

Article  PubMed  Google Scholar 

Wada, N. et al. High-resolution spatial and genomic characterization of coral-associated microbial aggregates in the coral Stylophora pistillata. Sci. Adv. 8, eabo2431 (2022).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Juhas, M., Crook, D. W. & Hood, D. W. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 10, 2377–2386 (2008).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lin, L., Lezan, E., Schmidt, A. & Basler, M. Abundance of bacterial type VI secretion system components measured by targeted proteomics. Nat. Commun. 10, 2584 (2019).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641–654 (2012).

Article  CAS  PubMed  Google Scholar 

Keller-Costa, T. et al. Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome. Microbiome 10, 151 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pollock, F. J., Morris, P. J., Willis, B. L. & Bourne, D. G. The urgent need for robust coral disease diagnostics. PLoS Pathog. 7, e1002183 (2011).

Article  PubMed  PubMed Central  Google Scholar 

Rosenberg, E. & Falkovitz, L. The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 58, 143–159 (2004).

Article  CAS  PubMed  Google Scholar 

Ben-Haim, Y., Zicherman-Keren, M. & Rosenberg, E. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 69, 4236–4242 (2003).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in southeastern Florida. Sci. Rep. 6, 31374 (2016).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in florida corals affected by stony coral tissue loss disease. Front. Mar. Sci. 8, 750658 (2021).

Article  Google Scholar 

Beavers, K. M. et al. Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae. Nat. Commun. 14, 2915 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Sweet, M. J. & Bulling, M. T. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4, 9 (2017).

Article  Google Scholar 

Vega Thurber, R. et al. Deciphering coral disease dynamics: integrating host, microbiome, and the changing environment. Front. Ecol. Evol. 8, 575927 (2020).

Article  Google Scholar 

Sato, Y., Civiello, M., Bell, S. C., Willis, B. L. & Bourne, D. G. Integrated approach to understanding the onset and pathogenesis of black band disease in corals. Environ. Microbiol. 18, 752–765 (2016).

Article  CAS  PubMed  Google Scholar 

Kvennefors, E. C. E. et al. Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb. Ecol. 63, 605–618 (2012).

Article  ADS  CAS  PubMed  Google Scholar 

Shnit-Orland, M., Sivan, A. & Kushmaro, A. Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb. Ecol. 64, 851–859 (2012).

Article  ADS  CAS  PubMed  Google Scholar 

Raina, J.-B. et al. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals. PeerJ 4, e2275 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Krediet, C. J., Ritchie, K. B., Alagely, A. & Teplitski, M. Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J. 7, 980–990 (2013).

Article  CAS  PubMed  Google Scholar 

Ushijima, B. et al. Chemical and genomic characterization of a potential probiotic treatment for stony coral tissue loss disease. Commun. Biol. 6, 248 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 17121 (2017).

Article  CAS  PubMed  Google Scholar 

Lesser, M. P., Bythell, J. C., Gates, R. D., Johnstone, R. W. & Hoegh-Guldberg, O. Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J. Exp. Mar. Biol. Ecol. 346, 36–44 (2007).

Article  Google Scholar 

Ezzat, L. et al. Parrotfish predation drives distinct microbial communities in reef-building corals. Anim. Microbiome 2, 5 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Hadaidi, G. et al. Ecological and molecular characterization of a coral black band disease outbreak in the Red Sea during a bleaching event. PeerJ 6, e5169 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Doering, T. et al. Towards enhancing coral heat tolerance: a “microbiome transplantation” treatment using inoculations of homogenized coral tissues. Microbiome 9, 102 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Moraïs, S. & Mizrahi, I. The road not taken: the rumen microbiome, functional groups, and community states. Trends Microbiol. 27, 538–549 (2019).

Article  PubMed  Google Scholar 

Thatcher, C., Høj, L. & Bourne, D. G. Probiotics for coral aquaculture: challenges and considerations. Curr. Opin. Biotechnol. 73, 380–386 (2022).

Article  CAS  PubMed  Google Scholar 

Barno, A. R., Villela, H. D. M., Aranda, M., Thomas, T. & Peixoto, R. S. Host under epigenetic control: a novel perspective on the interaction between microorganisms and corals. Bioessays 43, e2100068 (2021).

Article  PubMed  Google Scholar 

Costa, R. M. et al. Surface topography, bacterial carrying capacity, and the prospect of microbiome manipulation in the sea anemone coral model Aiptasia. Front. Microbiol. 12, 637834 (2021).

Article  PubMed  PubMed Central  Google Scholar 

Puntin, G. et al. The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research. Coral Reefs 42, 239–252 (2023).

Article  Google Scholar 

Kirsch, R. et al. Metabolic novelty originating from horizontal gene transfer is essential for leaf beetle survival. Proc. Natl Acad. Sci. USA 119, e2205857119 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tan, C. D. et al. The response of coral skeletal nano structure and hardness to ocean acidification conditions. R. Soc. Open Sci. 10, 230248 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Brown, B. E. Coral bleaching: causes and consequences. Coral Reefs 16, S129–S138 (1997).

Article  Google Scholar 

Johnston, E. C., Counsell, C. W. W., Sale, T. L., Burgess, S. C. & Toonen, R. J. The legacy of stress: coral bleaching impacts reproduction years later. Funct. Ecol. 34, 2315–2325 (2020).

Article  Google Scholar 

Palmer, C. V. Immunity and the coral crisis. Commun. Biol. 1, 91 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Pollock, F. J. et al. Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals. R. Soc. Open Sci. 6, 190355 (2019).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Röthig, R. et al. Human-induced salinity changes impact marine organisms and ecosystems. Glob. Chang. Biol. 29, 4731–4749 (2023).

Article  PubMed  Google Scholar 

Hughes, D. J. et al. Coral reef survival under accelerating ocean deoxygenation. Nat. Clim. Chang. 10, 296–307 (2020).

Article  ADS  CAS  Google Scholar 

Peixoto, R. S. & Voolstra, C. R. The baseline is already shifted: marine microbiome restoration and rehabilitation as essential tools to mitigate ecosystem decline. Front. Mar. Sci. 10, 1218531 (2023).

Article  Google Scholar 

Meron, D. et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51–60 (2011).

Article  PubMed  Google Scholar 

Renzi, J. J., Shaver, E. C., Burkepile, D. E. & Silliman, B. R. The role of predators in coral disease dynamics. Coral Reefs 41, 405–422 (2022).

Article  Google Scholar 

Kimes, N. E. et al. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J. 6, 835–846 (2012).

Article  CAS  PubMed  Google Scholar 

Boyett, H. V., Bourne, D. G. & Willis, B. L. Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef. Mar. Biol. 151, 1711–1720 (2007).

Article  Google Scholar 

Morrow, K. M. et al. Natural volcanic CO2 seeps reveal future trajectories for host–microbial associations in corals and sponges. ISME J. 9, 894–908 (2015).

Article  CAS  PubMed  Google Scholar 

Ezzat, L. et al. Surgeonfish feces increase microbial opportunism in reef-building corals. Mar. Ecol. Prog. Ser. 631, 81–97 (2019).

Article  ADS  CAS  Google Scholar 

Clever, F. et al. The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs. Commun. Biol. 5, 770 (2022).

Article  PubMed  PubMed Central  Google Scholar 

Nicolet, K. J., Chong-Seng, K. M., Pratchett, M. S., Willis, B. L. & Hoogenboom, M. O. Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease. Sci. Rep. 8, 5258 (2018).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Berg, G. & Cernava, T. The plant microbiota signature of the Anthropocene as a challenge for microbiome research. Microbiome 10, 54 (2022).

Article  PubMed  PubMed Central  Google Scholar 

Kang, D.-W. et al. Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota. Sci. Rep. 9, 5821 (2019).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Marinos, G. et al. Metabolic model predictions enable targeted microbiome manipulation through precision prebiotics. Microbiol. Spectr. 12, e0114423 (2024).

Article  PubMed  Google Scholar 

Grupstra, C. G. B., Lemoine, N. P., Cook, C. & Correa, A. M. S. Thank you for biting: dispersal of beneficial microbiota through ‘antagonistic’ interactions. Trends Microbiol. 30, 930–939 (2022).

Article  CAS  PubMed  Google Scholar 

Mills, J. G. et al. Urban habitat restoration provides a human health benefit through microbiome rewilding: the Microbiome Rewilding Hypothesis. Restor. Ecol. 25, 866–872 (2017).

Article  Google Scholar 

Dassi, E. et al. The short-term impact of probiotic consumption on the oral cavity microbiome. Sci. Rep. 8, 10476 (2018).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Merenstein, D. et al. Emerging issues in probiotic safety: 2023 perspectives. Gut Microbes 15, 2185034 (2023).

Article  PubMed  PubMed Central  Google Scholar 

Vanwonterghem, I. & Webster, N. S. Coral reef microorganisms in a changing climate. iScience 23, 100972 (2020).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Voolstra, C. R. et al. DNA preservation & DNA extraction protocol for field collection of coral samples suitable for host-, marker gene-, and metagenomics-based sequencing approaches. Zenodo https://doi.org/10.5281/zenodo.8124404 (2023).

Voolstra, C. R., Perna, G. & Alderdice, R. RNA preservation & RNA extraction protocol suitable for field collection of coral samples. Zenodo https://doi.org/10.5281/zenodo.7108092 (2022).

Voolstra, C. R. et al. Consensus guidelines for advancing coral holobiont genome and specimen voucher deposition. Front. Mar. Sci. 8, 1029 (2021).

Article  Google Scholar 

Staab, S., Cardenas, A., Peixoto, R., Schreiber, F. & Voolstra, C. R. Coracle — a machine learning framework to identify bacteria associated with continuous variables. Bioinformatics 40, btad749 (2024).

Article  PubMed  Google Scholar 

Garcias-Bonet, N. et al. Horizon scanning the application of probiotics for wildlife. Trends Microbiol. https://doi.org/10.1016/j.tim.2023.08.012 (2023).

de Lorenzo, V., Marlière, P. & Solé, R. Bioremediation at a global scale: from the test tube to planet Earth. Microb. Biotechnol. 9, 618–625 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Geller, A. M. & Levy, A. “What I cannot create, I do not understand”: elucidating microbe–microbe interactions to facilitate plant microbiome engineering. Curr. Opin. Microbiol. 72, 102283 (2023).

Article  PubMed  Google Scholar 

Ahkami, A. H., Allen White, R., Handakumbura, P. P. & Jansson, C. Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3, 233–243 (2017).

Article  Google Scholar 

Pandolfi, J. M. et al. Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958 (2003).

Article  ADS  CAS  PubMed  Google Scholar 

Pielke, R., Jr, Burgess, M. G. & Ritchie, J. Plausible 2005–2050 emissions scenarios project between 2 and 3 °C of warming by 2100. Environ. Res. Lett. 17, 024027 (2022).

Article  ADS  Google Scholar 

Hoegh-Guldberg, O., Kennedy, E. V., Beyer, H. L., McClennen, C. & Possingham, H. P. Securing a long-term future for coral reefs. Trends Ecol. Evol. 33, 936–944 (2018).

Article  PubMed  Google Scholar 

Voolstra, C. R., Peixoto, R. S. & Ferrier-Pagès, C. Mitigating the ecological collapse of coral reef ecosystems. EMBO Rep. 24, e56826 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Xiang, N. et al. Presence of algal symbionts affects denitrifying bacterial communities in the sea anemone Aiptasia coral model. ISME Commun. 2, 1–10 (2022).

Article  Google Scholar 

Matthews, J. L. et al. Coral endosymbiont growth is enhanced by metabolic interactions with bacteria. Nat. Commun. 14, 6864 (2023).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Raina, J. B. et al. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. eLife 6, e23008 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Sneed, J. M., Sharp, K. H., Ritchie, K. B. & Paul, V. J. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. R. Soc. B 281, 20133086 (2014).

Article  PubMed  PubMed Central  Google Scholar 

Diaz, J. M. et al. Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat. Commun. 7, 13801 (2016).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Motone, K. et al. A zeaxanthin-producing bacterium isolated from the algal phycosphere protects coral endosymbionts from environmental stress. mBio 11, e01019-19 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Ritchie, K. B. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322, 1–14 (2006).

Article  ADS  CAS  Google Scholar 

Ochsenkühn, M. A., Röthig, T., D’Angelo, C., Wiedenmann, J. & Voolstra, C. R. The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci. Adv.3, e1602047 (2017).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Epstein, H. E., Torda, G., Munday, P. L. & van Oppen, M. J. H. Parental and early life stage environments drive establishment of bacterial and dinoflagellate communities in a common coral. ISME J. 13, 1635–1638 (2019).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Williams, A. D., Brown, B. E., Putchim, L. & Sweet, M. J. Age-related shifts in bacterial diversity in a reef coral. PLoS ONE 10, e0144902 (2015).

Article  PubMed  PubMed Central  Google Scholar 

Wainwright, B. J., Zahn, G. L., Afiq-Rosli, L., Tanzil, J. T. I. & Huang, D. Host age is not a consistent predictor of microbial diversity in the coral Porites lutea. Sci. Rep. 10, 14376 (2020).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Quigley, K. M., Alvarez Roa, C., Torda, G., Bourne, D. G. & Willis, B. L. Co-dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles. Microbiology Open 9, e959 (2020).

Article  CAS  PubMed  Google Scholar 

Bernasconi, R. et al. Establishment of coral–bacteria symbioses reveal changes in the core bacterial community with host ontogeny. Front. Microbiol. 10, 1529 (2019).

Article  PubMed  PubMed Central  Google Scholar 

Galazzo, G. et al. How to count our microbes? The effect of different quantitative microbiome profiling approaches. Front. Cell. Infect. Microbiol. 10, 403 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bramucci, A. R., Focardi, A., Rinke, C. & Hugenholtz, P. Microvolume DNA extraction methods for microscale amplicon and metagenomic studies. ISME Commun. 1, 79 (2021).

Article  PubMed  PubMed Central  Google Scholar 

Duncan, K. D., Fyrestam, J. & Lanekoff, I. Advances in mass spectrometry based single-cell metabolomics. Analyst 144, 782–793 (2019).

Article  ADS  CAS  PubMed  Google Scholar 

Assis, J. M. et al. Delivering beneficial microorganisms for corals: rotifers as carriers of probiotic bacteria. Front. Microbiol. 11, 608506 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Mostafa, H. Lyophilized probiotic lactic acid bacteria viability in potato chips and its impact on oil oxidation. Foods 9, 586 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kiepś, J. & Dembczyński, R. Current trends in the production of probiotic formulations. Foods 11, 2330 (2022).

Article  PubMed  PubMed Central  Google Scholar 

Wood-Charlson, E. M., Weynberg, K. D., Suttle, C. A., Roux, S. & van Oppen, M. J. H. Metagenomic characterization of viral communities in corals: mining biological signal from methodological noise. Environ. Microbiol. 17, 3440–3449 (2015).

Article  PubMed  Google Scholar 

Levin, R. A., Voolstra, C. R., Weynberg, K. D. & van Oppen, M. J. H. Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J. 11, 808–812 (2017).

Article  CAS  PubMed  Google Scholar 

Simmonds, P. et al. Four principles to establish a universal virus taxonomy. PLoS Biol. 21, e3001922 (2023).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Weynberg, K. D., Voolstra, C. R., Neave, M. J., Buerger, P. & van Oppen, M. J. H. From cholera to corals: viruses as drivers of virulence in a major coral bacterial pathogen. Sci. Rep. 5, 17889 (2015).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Rubio-Portillo, E. et al. Virulence as a side effect of interspecies interaction in vibrio coral pathogens. mBio 11, e00201-20 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Buerger, P. et al. Novel T4 bacteriophages associated with black band disease in corals. Environ. Microbiol. 21, 1969–1979 (2019).

Article  CAS  PubMed  Google Scholar 

Wang, W. et al. The coral pathogen Vibrio coralliilyticus kills non-pathogenic holobiont competitors by triggering prophage induction. Nat. Ecol. Evol. 6, 1132–1144 (2022).

Article  PubMed  Google Scholar 

Roach, T. N. F. et al. A multiomic analysis of in situ coral–turf algal interactions. Proc. Natl Acad. Sci. USA 117, 13588–13595 (2020).

Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Silveira, C. B. & Rohwer, F. L. Piggyback-the-winner in host-associated microbial communities. npj Biofilms Microbiomes 2, 16010 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Silveira, C. B. et al. Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes. BMC Genomics 21, 126 (2020).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cohen, Y., Joseph Pollock, F., Rosenberg, E. & Bourne, D. G. Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. Microbiologyopen 2, 64–74 (2013).

Article  CAS  PubMed  Google Scholar 

Dinsdale, E. A. et al. Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 3, e1584 (2008).

Article  ADS  PubMed  PubMed Central  Google Scholar 

Nelson, C. E., Wegley Kelly, L. & Haas, A. F. Microbial interactions with dissolved organic matter are central to coral reef ecosystem function and resilience. Ann. Rev. Mar. Sci. 15, 431–460 (2023).

Article  PubMed  Google Scholar 

Sil