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Naturally occurring fire coral clones demonstrate a genetic and environmental basis of microbiome composition

  • 1.

    McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 2.

    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–9 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 3.

    Mueller, U. G. & Sachs, J. L. Engineering microbiomes to improve plant and animal health. Trends Microbiol. 23, 606–617 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 4.

    Theis, K. R., Whittaker, D. J. & Rojas, C. A. A hologenomic approach to animal behavior. In Evolution in Action: Past, Present and Future 247–263 (Springer, 2020).

  • 5.

    Foster, K. R., Schluter, J., Coyte, K. Z. & Rakoff-Nahoum, S. The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    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, 1–8 (2017).

    Article 
    CAS 

    Google Scholar 

  • 7.

    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).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 8.

    Berendsen, R. L., Pieterse, C. M. & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Voolstra, C. R. & Ziegler, M. Adapting with microbial help: Microbiome flexibility facilitates rapid responses to environmental change. BioEssays 2, 2000004 (2020).

    Article 

    Google Scholar 

  • 10.

    Cárdenas, C. A., Bell, J. J., Davy, S. K., Hoggard, M. & Taylor, M. W. Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol. Ecol. 88, 516–527 (2014).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 11.

    Pantos, O., Bongaerts, P., Dennis, P. G., Tyson, G. W. & Hoegh-Guldberg, O. Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J. 9, 1916–1927 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 12.

    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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 13.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 14.

    Carrier, T. J. & Reitzel, A. M. Convergent shifts in host-associated microbial communities across environmentally elicited phenotypes. Nat. Commun. 9, 1–9 (2018).

    CAS 
    Article 

    Google Scholar 

  • 15.

    Pollock, F. J. et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9, 1–13 (2018).

    CAS 
    Article 

    Google Scholar 

  • 16.

    Glasl, B., Smith, C. E., Bourne, D. G. & Webster, N. S. Disentangling the effect of host-genotype and environment on the microbiome of the coral Acropora tenuis. PeerJ 7, e6377 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 17.

    Macke, E., Callens, M., De Meester, L. & Decaestecker, E. Host-genotype dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nat. Commun. 8, 1–13 (2017).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Casey, J. M., Connolly, S. R. & Ainsworth, T. D. Coral transplantation triggers shift in microbiome and promotion of coral disease associated potential pathogens. Sci. Rep. 5, 11903 (2015).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 19.

    Ziegler, M. et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 1–11 (2019).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 20.

    Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 21.

    Spor, A., Koren, O. & Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 23.

    Jaspers, C. et al. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. Zoology 113, 81–87 (2019).

    Article 

    Google Scholar 

  • 24.

    Blackall, L. L., Wilson, B. & van Oppen, M. J. H. Coral—the world’s most diverse symbiotic ecosystem. Mol. Ecol. 24, 5330–5347 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 25.

    Hernandez-Agreda, A., Gates, R. D. & Ainsworth, T. D. Defining the core microbiome in corals’ microbial soup. Trends Microbiol. 25, 125–140 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 26.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 27.

    Rohwer, F., Seguritan, V., Azam, F. & Knowlton, N. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243, 1–10 (2002).

    ADS 
    Article 

    Google Scholar 

  • 28.

    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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 30.

    Muscatine, L., Porter, J. W. & Kaplan, I. R. Resource partitioning by reef corals as determined from stable isotope composition. Mar. Biol. 100, 185–193 (1989).

    Article 

    Google Scholar 

  • 31.

    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).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 32.

    Wegley, L., Edwards, R., Rodriguez‐Brito, B., Liu, H. & Rohwer, F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9, 2707–2719 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 33.

    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).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 34.

    Lema, K. A., Willis, B. L. & Bourne, D. G. Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 78, 3136–3144 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 35.

    Krediet, C. J., Ritchie, K. B., Paul, V. J. & Teplitski, M. Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc. R. Soc. B 280, 20122328 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 36.

    Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280–2292 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Boilard, A. et al. Defining coral bleaching as a microbial dysbiosis within the coral holobiont. Microorganisms 8, 1682 (2020).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • 38.

    Apprill, A., Weber, L. G. & Santoro, A. E. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems 1, e00143–16 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 39.

    Glasl, E.B., B. et al. Microbial indicators of environmental perturbations in coral reef ecosystems. Microbiome 7, 1–13 (2019).

    Article 

    Google Scholar 

  • 40.

    Damjanovic, K., Blackall, L. L., Peplow, L. M. & van Oppen, M. J. H. Assessment of bacterial community composition within and among Acropora loripes colonies in the wild and in captivity. Coral Reefs 39, 1245–1255 (2020).

    Article 

    Google Scholar 

  • 41.

    Dubé, E. B. et al. Ecology, biology and genetics of Millepora hydrocorals on coral reefs. In Invertebrates – Ecophysiology and Management (eds. Ray, S., Diarte-Plata, G. &  Escamilla-Montes, R.), (IntechOpen, 2019).

  • 42.

    Rodríguez, L. et al. Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic. Coral Reefs 38, 255–268 (2019).

    ADS 
    Article 

    Google Scholar 

  • 43.

    Lewis, J. B. Biology and ecology of the hydrocoral Millepora on coral reefs. Adv. Mar. Biol. 50, 1–55 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 44.

    Arrigoni, R. et al. An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea. Coral Reefs 37, 967–984 (2018).

    ADS 
    Article 

    Google Scholar 

  • 45.

    Boissin, E., Leung, J. K., Denis, V., Bourmaud, C. A. & Gravier-Bonnet, N. Morpho-molecular delineation of structurally important reef species, the fire corals, Millepora spp., at Réunion Island, Southwestern Indian Ocean. Hydrobiologia 847, 1237–1255 (2020).

    Article 

    Google Scholar 

  • 46.

    Dubé, C. E., Boissin, E., Maynard, J. A. & Planes, S. Fire coral clones demonstrate phenotypic plasticity among reef habitats. Mol. Ecol. 26, 3860–3869 (2017).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 47.

    Schwartzman, J. A. & Ruby, E. G. Stress as a normal cue in the symbiotic environment. Trends Microbiol. 24, 414–424 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 48.

    van Oppen, M. J. H. et al. Adaptation to reef habitats through selection on the coral animal and its associated microbiome. Mol. Ecol. 27, 2956–2971 (2018).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 49.

    Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 6237 (2015).

    Article 
    CAS 

    Google Scholar 

  • 50.

    Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 51.

    Hernandez-Agreda, A., Leggat, W., Bongaerts, P., Herrera, C. & Ainsworth, T. D. Rethinking the coral microbiome: simplicity exists within a diverse microbial biosphere. MBio 9, e00812–18 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 52.

    Bongaerts, P. et al. Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol. Biol. 11, 303 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Albright, R., Benthuysen, J., Cantin, N., Caldeira, K. & Anthony, K. Coral reef metabolism and carbon chemistry dynamics of a coral reef flat. Geophys. Res. Lett. 42, 3980–3988 (2015).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 54.

    Pootakham, W. et al. Dynamics of coral‐associated microbiomes during a thermal bleaching event. MicrobiologyOpen 7, e00604 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 55.

    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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Meyer, J. L., Paul, V. J. & Teplitski, M. Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS ONE 9, e100316 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Bayer, T. et al. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79, 4759–4762 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Jessen, C. et al. In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS ONE 8, e62091 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 59.

    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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 60.

    Dubé, C. E., Ky, C. L. & Planes, S. Microbiome of the black-lipped pearl oyster Pinctada margaritifera, a multi-tissue description with functional profiling. Front. Microbiol. 10, 1548 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 61.

    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).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 62.

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

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 63.

    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).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    González, J. M., Kiene, R. P. & Moran, M. A. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl. Environ. Microbiol. 65, 3810–3819 (1999).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 65.

    Curson, A. R. J., Rogers, R., Todd, J. D., Brearley, C. A. & Johnston, A. W. B. Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter spharoides. Environ. Microbiol. 10, 757–767 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 66.

    Reisch, C. R., Moran, M. A. & Whitman, W. B. Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front. Microbiol. 2, 172 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 67.

    Thompson, J. R., Rivera, H. E., Closek, C. J. & Medina, M. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front. Cell. Infect. Microbiol. 4, 176 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 68.

    Durante, M. K., Baums, I. B., Williams, D. E., Vohsen, S. & Kemp, D. W. What drives phenotypic divergence among coral clonemates of Acropora palmata? Mol. Ecol. 28, 3208–3224 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 69.

    Wagner, M. R. et al. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 7, 1–5 (2016).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 70.

    Fuerst, J. & Sagulenko, E. Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat. Rev. Microbiol. 9, 403–413 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Forquin-Gomez, M. P. et al. The family Brevibacteriaceae. In Prokaryotes Actinobacteria. 4th edn., (eds. Rosenberg E. et al.), 141–153 (Springer, 2014).

  • 72.

    Baker, B. J., Lazar, C. S., Teske, A. P. & Dick, G. J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3, 14 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 73.

    Tian, R. M. et al. Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur‐oxidizing bacterium in sponge. Environ. Microbiol. 16, 3548–3561 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 74.

    Gauthier, M. E., Watson, J. R. & Degnan, S. M. Draft genomes shed light on the dual bacterial symbiosis that dominates the microbiome of the coral reef sponge Amphimedon queenslandica. Front. Mar. Sci. 3, 196 (2016).

    Article 

    Google Scholar 

  • 75.

    Dyksma, S. et al. Ubiquitous Gammaproteo-bacteria dominate dark carbon fixation in coastal sediments. ISME J. 8, 1939–1953 (2016).

    Article 
    CAS 

    Google Scholar 

  • 76.

    Raina, J. B., Dinsdale, E. A., Willis, B. L. & Bourne, D. G. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 18, 101–108 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 77.

    Morrow, K. M., Moss, A. G., Chadwick, N. E. & Liles, M. R. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl. Environ. Microbiol. 78, 6438–6449 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 78.

    Sabdono, A. & Radjasa, O. K. Phylogenetic diversity of organophosphorous pesticide-degrading coral bacteria from mid-west coast of Indonesia. Biotechnology 7, 694–701 (2008).

    CAS 
    Article 

    Google Scholar 

  • 79.

    Kannapiran, E. & Ravindran, J. Dynamics and diversity of phosphate mineralizing bacteria in the coral reefs of Gulf of Mannar. J. Basic Microbiol. 52, 91–98 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 80.

    Mahmoud, H. M. & Kalendar, A. A. Coral-associated actinobacteria: diversity, abundance, and biotechnological potentials. Front. Microbiol. 7, 204 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 81.

    Probandt, D. et al. Permeability shapes bacterial communities in sublittoral surface sediments. Environ. Microbiol. 19, 1584–1599 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 82.

    Doolittle, W. F. & Booth, A. It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol. Philos. 32, 5–24 (2017).

    Article 

    Google Scholar 

  • 83.

    Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 84.

    Kelly, L. W. et al. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc. Natl Acad. Sci. USA 111, 10227–10232 (2014).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 85.

    Peixoto, R. S., Rosado, P. M., Leite, D. C. D. A., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 341 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 86.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 87.

    Voolstra, C. R. et al. Extending the natural adaptive capacity of coral holobionts. Nat Rev Earth Environ. 1–16 (2021). https://doi.org/10.1038/s43017-021-00214-3.

  • 88.

    Santoro, E. P. et al. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci Adv. 7 (2021). https://doi.org/10.1126/sciadv.abg3088.

  • 89.

    Adam, T. C. et al. Landscape‐scale patterns of nutrient enrichment in a coral reef ecosystem: implications for coral to algae phase shifts. Ecol. Appl. 31, e2227 (2021).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 90.

    Buckling, A., Kassen, R., Bell, G. & Rainey, P. B. Disturbance and diversity in experimental microcosms. Nature 408, 961–964 (2000).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 91.

    Berga, M., Szekely, A. J. & Langenheder, S. Effects of disturbance intensity and frequency on bacterial community composition and function. PLoS ONE 7, e36959 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 92.

    Neulinger, S. C., Järnegren, J., Ludvigsen, M., Lochte, K. & Dullo, W. C. Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral’s nutrition, health, and distribution. Appl. Environ. Microbiol. 74, 7272–7285 (2008).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 93.

    Kanukollu, S. et al. Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol. Ecol. 92, 1 (2016).

    Article 
    CAS 

    Google Scholar 

  • 94.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 95.

    Sorokin, D. Y., Tourova, T. P. & Muyzer, G. Citreicella thiooxidans gen. nov., sp. nov., a novel lithoheterotrophic sulfur-oxidizing bacterium from the Black Sea. Syst. Appl. Microbiol. 28, 679–687 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 96.

    Chen, Y. J. et al. Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem. bioRxiv (2020). Preprint at https://doi.org/10.1101/2020.02.12.945220

  • 97.

    Spring, S., Scheuner, C., Göker, M. & Klenk, H. P. A taxonomic framework for emerging groups of ecologically important marine gammaproteobacteria based on the reconstruction of evolutionary relationships using genome-scale data. Front. Microbiol. 9, 281 (2015).

    Google Scholar 

  • 98.

    Preston, G. M. Metropolitan microbes: type III secretion in multi-host symbionts. Cell Host Microbe 2, 291–294 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 99.

    Lutz, A., Raina, J.-B., Motti, C. A., Miller, D. J. & van Oppen, M. J. H. Host coenzyme Q redox state is an early biomarker of thermal stress in the coral Acropora millepora. PLoS ONE 10, e0139290 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 100.

    Smith, D. J., Suggett, D. J. & Baker, N. R. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Glob. Chang. Biol. 11, 1–11 (2005).

    ADS 
    Article 

    Google Scholar 

  • 101.

    Gardner, S. G. et al. A multi-trait systems approach reveals a response cascade to bleaching in corals. BMC Biol. 15, 1–14 (2017).

    Article 
    CAS 

    Google Scholar 

  • 102.

    Lema, K. A., Bourne, D. G. & Willis, B. L. Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora. Mol. Ecol. 23, 4682–4695 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 104.

    Marangoni, L. F. et al. Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral–dinoflagellate symbiosis in a scleractinian and hydrocoral species. Microorganisms 7, 426 (2019).

    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 105.

    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. MicrobiologyOpen 9, e959 (2020).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 106.

    Dubé, C. E., Mercière, A., Vermeij, M. J. A. & Planes, S. Population structure of the hydrocoral Millepora platyphylla in habitats experiencing different flow regimes in Moorea, French Polynesia. PLoS ONE 12, e0173513 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 107.

    Agostini, S. et al. Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31, 147–156 (2012).

    ADS 
    Article 

    Google Scholar 

  • 108.

    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).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 109.

    Sweet, M. J., Brown, B. E., Dunne, R. P., Singleton, I. & Bulling, M. Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera. Coral Reefs 36, 815–828 (2017).

    ADS 
    Article 

    Google Scholar 

  • 110.

    Dubé, C. E., Boissin, E., Mercière, A. & Planes, S. Parentage analyses identify local dispersal events and sibling aggregations in a natural population of Millepora hydrocorals, a free‐spawning marine invertebrate. Mol. Ecol. 29, 1508–1522 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 111.

    Abràmoff, M. D., Magalhães, P. J. & Ram, S. J. Image processing with ImageJ. Biophotonics Int. 11, 36–42 (2004).

    Google Scholar 

  • 112.

    Dubé, C. E., Planes, S., Zhou, Y., Berteaux-Lecellier, V. & Boissin, E. Genetic diversity and differentiation in reef-building Millepora species, as revealed by cross-species amplification of fifteen novel microsatellite loci. PeerJ 5, e2936 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 113.

    Arnaud-Haond, S. & Belkhir, K. GENCLONE: A computer pro- gram to analyze genotypic data, test for clonality and describe spatial clonal organization. Mol. Ecol. Notes 7, 15–17 (2007).

    CAS 
    Article 

    Google Scholar 

  • 114.

    Peakall, R. & Smouse, P. E. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295 (2006).

    Article 

    Google Scholar 

  • 115.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer, 2016).

  • 116.

    R Development Core Team. R: A language and environment for statistical computing (ISBN 3-900051-07-0, http://www.R-project.org/ (R Foundation for Statistical Computing, 2020).

  • 117.

    Andersson, A. F. et al. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PloS ONE 3, e2836 (2008).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 118.

    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 119.

    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 120.

    Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 121.

    Pedregosa, F. et al. Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 12, 2825–2830 (2011).

    MathSciNet 
    MATH 

    Google Scholar 

  • 122.

    Bokulich, N. A. et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6, 1–17 (2018).

    Article 

    Google Scholar 

  • 123.

    Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucl. Acids Res. 42, D643–D648 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 124.

    Oksanen, J. et al. vegan: Community Ecology Package (2018).

  • 125.

    Weerdt, W. H. Transplantation experiments with Caribbean Millepora species (Hydrozoa, Coelenterata), including some ecological observations on growth forms. Bijdr. Dierkd. 51, 1–19 (1981).

    Article 

    Google Scholar 

  • 126.

    Cáceres, M. D. & Legendre, P. Associations between species and groups of sites: indices and statistical inference. Ecology 90, 3566–3574 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 127.

    Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 128.

    Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 


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