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

Nature Reviews Microbiology (2024)Cite this article

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Abstract

Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately, coral death. Although progress has been made in characterizing the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.

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Fig. 1: Coral and bacterial microbiome diversity.
Fig. 2: Bacterial colonization and succession of corals over their life stages.
Fig. 3: Coral health in a changing world and the role of the microbiome for reef conservation and management.

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References

  1. 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 

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

  3. 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 

  4. 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 

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

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

    Google Scholar 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. 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 

  15. 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 

  16. 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 

  17. 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 

  18. 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 

  19. 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 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  22. 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 

  23. 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 

  24. 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 

  25. 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 

  26. 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 

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

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  28. 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 

  29. 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 

  30. 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 

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

    Article  PubMed  Google Scholar 

  32. 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 

  33. 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 

  34. 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 

  35. 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 

  36. 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 

  37. 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 

  38. 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 

  39. 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 

  40. 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 

  41. 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 

  42. 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 

  43. 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 

  44. 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 

  45. 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 

  46. 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 

  47. 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 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

  52. 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 

  53. 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 

  54. 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 

  55. 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 

  56. 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 

  57. 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 

  58. 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 

  59. 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 

  60. 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 

  61. 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 

  62. 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 

  63. 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 

  64. 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 

  65. 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 

  66. 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 

  67. 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 

  68. 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 

  69. 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 

  70. 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 

  71. 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 

  72. 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 

  73. 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 

  74. 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 

  75. 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 

  76. 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 

  77. 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 

  78. 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 

  79. 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 

  80. 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 

  81. 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 

  82. 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).

  83. 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 

  84. 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 

  85. 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 

  86. 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 

  87. 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 

  88. 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 

  89. 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 

  90. 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 

  91. 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 

  92. 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 

  93. 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 

  94. 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 

  95. 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 

  96. 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 

  97. 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 

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

    Article  PubMed  Google Scholar 

  99. 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 

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

    Article  CAS  PubMed  Google Scholar 

  101. 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 

  102. 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 

  103. 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 

  104. 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 

  105. 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 

  106. 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 

  107. 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 

  108. 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 

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

    Article  ADS  CAS  Google Scholar 

  110. 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 

  111. 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 

  112. 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 

  113. 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 

  114. 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 

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

    Article  Google Scholar 

  116. 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 

  117. 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 

  118. 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 

  119. 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 

  120. 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 

  121. 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 

  122. 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 

  123. 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 

  124. 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 

  125. 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 

  126. 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 

  127. 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 

  128. 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 

  129. 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 

  130. 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 

  131. 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 

  132. 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 

  133. 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 

  134. 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 

  135. 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 

  136. 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 

  137. 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 

  138. 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 

  139. 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 

  140. 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 

  141. 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 

  142. 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 

  143. 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 

  144. 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 

  145. 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 

  146. 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 

  147. 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 

  148. 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 

  149. 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 

  150. 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 

  151. 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 

  152. 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 

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

    Article  Google Scholar 

  154. 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  156. 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 

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

    Article  PubMed  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  159. 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 

  160. 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 

  161. 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 

  162. 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 

  163. 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 

  164. 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 

  165. 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 

  166. 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 

  167. 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 

  168. 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 

  169. 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 

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

    Article  PubMed  Google Scholar 

  171. 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 

  172. 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 

  173. 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  176. 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).

  177. 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).

  178. 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 

  179. 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 

  180. 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).

  181. 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 

  182. 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 

  183. 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 

  184. 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 

  185. 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 

  186. 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 

  187. 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 

  188. 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 

  189. 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 

  190. 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 

  191. 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 

  192. 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 

  193. 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 

  194. 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 

  195. 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 

  196. 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 

  197. 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 

  198. 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 

  199. 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 

  200. 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 

  201. 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 

  202. 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 

  203. 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 

  204. 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 

  205. 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  207. 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 

  208. 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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. 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 

  211. 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 

  212. 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 

  213. 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 

  214. 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 

  215. 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 

  216. 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 

  217. 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 

  218. 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 

  219. 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 

  220. Silveira, C. B. et al. Viral predation pressure on coral reefs. BMC Biol. 21, 77 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  221. Silveira, C. B. et al. Bacterial community associated with the reef coral Mussismilia braziliensis’s momentum boundary layer over a diel cycle. Front. Microbiol. 8, 784 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  222. Knowles, B. et al. Lytic to temperate switching of viral communities. Nature 531, 466–470 (2016).

    Article  ADS  CAS  PubMed  Google Scholar 

  223. Buerger, P., Wood-Charlson, E. M., Weynberg, K. D., Willis, B. L. & van Oppen, M. J. H. CRISPR–Cas defense system and potential prophages in cyanobacteria associated with the coral black band disease. Front. Microbiol. 7, 2077 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

C.R.V. acknowledges support by Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) project numbers 433042944, 458901010 and 468583787. J.-B.R. is supported by an Australian Research Council Fellowship (FT210100100). C.P. is supported by a Junior Professorship Grant from Agence National de la Recherche (ANR; French National Research Agency) project number ANR-22-CPJ2-0113-01 and an associated start-up grant from the Institut Écologie et Environnement (INEE; Ecology and Environment Institute) of the Centre National de la Recherche Scientifique (CNRS; French National Centre for Scientific Research). R.S.P. acknowledges funding provided by KAUST (BAS/1/1095-01-01 and FCC/1/1976-40-01). S.A.A. is supported by Tamkeen under the NYU Abu Dhabi Research Institute Award to the NYUAD Center for Genomics and Systems Biology (ADHPG-CGSB). C.B.S. acknowledges funding provided by the NASA Exobiology Program (80NSSC23K0676). C.R.V. and R.S.P. acknowledge funding from KAUST (OSR-2021-NTGC-4984).

Author information

Author notes

  1. These authors contributed equally: Christian R. Voolstra, Jean-Baptiste Raina.

Authors and Affiliations

  1. Department of Biology, University of Konstanz, Konstanz, Germany

    Christian R. Voolstra & Melanie Dörr

  2. Climate Change Cluster, University of Technology Sydney, Ultimo, New South Wales, Australia

    Jean-Baptiste Raina

  3. Department of Biology, American University, Washington, DC, USA

    Anny Cárdenas

  4. PSL Université Paris: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Université de Perpignan, Perpignan, France

    Claudia Pogoreutz

  5. Department of Biology, University of Miami, Coral Gables, FL, USA

    Cynthia B. Silveira

  6. Marine Microbiomics Laboratory, Biology Program, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Amin R. Mohamed & Shady A. Amin

  7. Australian Institute of Marine Science, Townsville, Queensland, Australia

    David G. Bourne

  8. College of Science and Engineering, James Cook University, Townsville, Queensland, Australia

    David G. Bourne

  9. Simon F.S. Li Marine Science Laboratory, School of Life Sciences, State Key Laboratory of Agrobiotechnology and Institute of Environment, Energy and Sustainability, The Chinese University of Hong Kong, Hong Kong SAR, China

    Haiwei Luo

  10. Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Shady A. Amin

  11. Red Sea Research Center (RSRC) and Computational Biology Research Center (CBRC), Biological, Environmental Sciences, and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    Raquel S. Peixoto

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  1. Christian R. Voolstra
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Contributions

C.R.V., R.S.P. and J.-B.R. researched data for the article, substantially contributed to discussion of content, wrote the article, and reviewed and edited the manuscript before submission. D.G.B. substantially contributed to discussion of content, and reviewed and edited the manuscript before submission. A.C., C.P., H.L., A.R.M., S.A.A. and C.B.S. researched data for the article, wrote the article, and reviewed and edited the manuscript before submission. C.R.V. conceived and, with M.D., designed the figures. M.D. illustrated the draft figures, wrote the article, and reviewed and edited the manuscript before submission.

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Correspondence to Christian R. Voolstra, Jean-Baptiste Raina or Raquel S. Peixoto.

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Nature Reviews Microbiology thanks Adrienne Correa, Blake Ushijima and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Voolstra, C.R., Raina, JB., Dörr, M. et al. The coral microbiome in sickness, in health and in a changing world. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01015-3

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