in

The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs

[adace-ad id="91168"]
  • Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F. & Bronstein, J. L. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13, 1459–1474 (2010).

    Article 

    Google Scholar 

  • Idjadi, J. & Edmunds, P. Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar. Ecol. Prog. Ser. 319, 117–127 (2006).

    Article 

    Google Scholar 

  • Norström, A., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 295–306 (2009).

    Article 

    Google Scholar 

  • Richardson, L. E., Graham, N. A. J., Pratchett, M. S., Eurich, J. G. & Hoey, A. S. Mass coral bleaching causes biotic homogenization of reef fish assemblages. Glob. Chang. Biol. 24, 3117–3129 (2018).

    PubMed 
    Article 

    Google Scholar 

  • Wilson, S. K., Graham, N. A. J., Pratchett, M. S., Jones, G. P. & Polunin, N. V. C. Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob. Chang. Biol. 12, 2220–2234 (2006).

    Article 

    Google Scholar 

  • Apprill, A. The role of symbioses in the adaptation and stress responses of marine organisms. Ann. Rev. Mar. Sci. 12, 291–314 (2020).

  • Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do Vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31, 689–699 (2016).

    PubMed 
    Article 

    Google Scholar 

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

  • Webster, N. S. & Reusch, T. B. H. Microbial contributions to the persistence of coral reefs. ISME J. 11, 2167–2174 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wilkins, L. G. E. et al. Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol. 17, e3000533 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776–788 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Egerton, S., Culloty, S., Whooley, J., Stanton, C. & Ross, R. P. The gut microbiota of marine fish. Front. Microbiol. 9, 873 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Llewellyn, M. S., Boutin, S., Hoseinifar, S. H. & Derome, N. Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front. Microbiol. 5, 1–1 (2014).

    Article 

    Google Scholar 

  • Tarnecki, A. M., Burgos, F. A., Ray, C. L. & Arias, C. R. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J. Appl. Microbiol. 123, 2–17 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wang, A. R., Ran, C., Ringø, E. & Zhou, Z. G. Progress in fish gastrointestinal microbiota research. Rev. Aquac. 10, 626–640 (2018).

    Article 

    Google Scholar 

  • Legrand, T. P. R. A., Wynne, J. W., Weyrich, L. S. & Oxley, A. P. A. A microbial sea of possibilities: current knowledge and prospects for an improved understanding of the fish microbiome. Rev. Aquac. 12, 1101–1134 (2019).

  • Rawls, J. F., Mahowald, M. A., Ley, R. E. & Gordon, J. I. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423–433 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Shade, A. & Handelsman, J. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4–12 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sullam, K. E. et al. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol. 21, 3363–3378 (2012).

    PubMed 
    Article 

    Google Scholar 

  • Ainsworth, T. D. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261–2274 (2015).

    CAS 
    Article 

    Google Scholar 

  • Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio. 7, e00560–16 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Roeselers, G. et al. Evidence for a core gut microbiota in the zebrafish. ISME J. 5, 1595–1608 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Clements, K. D., Angert, E. R., Montgomery, W. L. & Choat, J. H. Intestinal microbiota in fishes: what’s known and what’s not. Mol. Ecol. 23, 1891–1898 (2014).

    PubMed 
    Article 

    Google Scholar 

  • Jones, J. et al. The microbiome of the gastrointestinal tract of a range-shifting marine herbivorous fish. Front. Microbiol. 9, 2000 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Miyake, S., Ngugi, D. K. & Stingl, U. Diet strongly influences the gut microbiota of surgeonfishes. Mol. Ecol. 24, 656–672 (2015).

    PubMed 
    Article 

    Google Scholar 

  • Ngugi, D. K. et al. Genomic diversification of giant enteric symbionts reflects host dietary lifestyles. Proc. Natl Acad. Sci. USA 114, E7592–E7601 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Degregori, S., Casey, J. M. & Barber, P. H. Nutrient pollution alters the gut microbiome of a territorial reef fish. Mar. Pollut. Bull. 169, 112522 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gómez, G. D. & Balcázar, J. L. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol. 52, 145–154 (2008).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Butt, R. L. & Volkoff, H. Gut microbiota and energy homeostasis in fish. Front. Endocrinol. 10, 9 (2019).

    Article 

    Google Scholar 

  • Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bellwood, D. R. et al. Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. J. Evol. Biol. 23, 335–349 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Berumen, M., S., M. & McCormick, M. Within-reef differences in diet and body condition of coral-feeding butterflyfishes (Chaetodontidae). Mar. Ecol. Prog. Ser. 287, 217–227 (2005).

    Article 

    Google Scholar 

  • Pratchett, M. S. Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar. Biol. 148, 373–382 (2005).

    Article 

    Google Scholar 

  • Nagelkerken, I., van der Velde, G., Wartenbergh, S. L. J., Nugues, M. M. & Pratchett, M. S. Cryptic dietary components reduce dietary overlap among sympatric butterflyfishes (Chaetodontidae). J. Fish. Biol. 75, 1123–1143 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bouchon & Harmelin-Vivien Impact of coral degradation on a chaetodontid fish assemblage, Moorea, French Polynesia. Fifth Int. Coral Tahiti 5, 427–432 (1985).

    Google Scholar 

  • Graham, N. A. J. Ecological versatility and the decline of coral feeding fishes following climate driven coral mortality. Mar. Biol. 153, 119–127 (2007).

    Article 

    Google Scholar 

  • Pratchett, M. S., Wilson, S. K. & Baird, A. H. Declines in the abundance of Chaetodon butterflyfishes following extensive coral depletion. J. Fish. Biol. 69, 1269–1280 (2006).

    Article 

    Google Scholar 

  • Birkeland & Neudecker. Foraging behavior of two Caribbean Chaetodontids: Chaetodon capistratus and C. aculeatus. Copeia 1981, 169–178 (1981).

  • Gore, M. A. Factors affecting the feeding behavior of a coral reef fish, Chaetodon capistratus. Bull. Mar. Sci. 35, 211–220 (1984).

    Google Scholar 

  • Liedke, A. M. R. et al. Resource partitioning by two syntopic sister species of butterflyfish (Chaetodontidae). J. Mar. Biol. Assoc. UK 98, 1767–1773 (2018).

    CAS 
    Article 

    Google Scholar 

  • Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl Acad. Sci. USA 114, 3660–3665 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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).

    CAS 
    PubMed 
    Article 

    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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ricaboni, D., Mailhe, M., Khelaifia, S., Raoult, D. & Million, M. Romboutsia timonensis, a new species isolated from human gut. N. Microbes N. Infect. 12, 6–7 (2016).

    CAS 
    Article 

    Google Scholar 

  • Zhang, L. et al. Characterization of the microbial community structure in intestinal segments of yak (Bos grunniens). Anaerobe 61, 102115 (2020).

  • Gerritsen, J. et al. A comparative and functional genomics analysis of the genus Romboutsia provides insight into adaptation to an intestinal lifestyle. Preprint at bioRxiv https://doi.org/10.1101/845511 (2019).

  • Fernández-Cadena, J. C. et al. Detection of sentinel bacteria in mangrove sediments contaminated with heavy metals. Mar. Pollut. Bull. 150, 110701 (2020).

  • Williams, B., Landay, A. & Presti, R. M. Microbiome alterations in HIV infection a review. Cell. Microbiol. 18, 645–651 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ahmed, H. I., Herrera, M., Liew, Y. J. & Aranda, M. Long-term temperature stress in the Coral Model Aiptasia supports the ‘Anna Karenina principle’ for bacterial microbiomes. Front. Microbiol. 10, 975 (2019).

  • Beatty, D. S. et al. Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen. Sci. Adv. 5, eaay1048 (2019).

  • Zaneveld, J. R. et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7, 11833 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ma, Q. et al. Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. J. Neuroinflammation 16, 53 (2019).

  • Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6, 46 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Johnson, K. V. A. & Foster, K. R. Why does the microbiome affect behaviour? Nat. Rev. Microbiol. 16, 647–655 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Werbner, M. et al. Social-stress-responsive microbiota induces stimulation of self-reactive effector T helper cells. mSystems 4, e00292-18 (2019).

  • Keith, S. A. et al. Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nat. Clim. Chang. 8, 986–991 (2018).

    Article 

    Google Scholar 

  • Thompson, C. A., Matthews, S., Hoey, A. S. & Pratchett, M. S. Changes in sociality of butterflyfishes linked to population declines and coral loss. Coral Reefs 38, 527–537 (2019).

    Article 

    Google Scholar 

  • Almany, G. R. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141, 105–113 (2004).

    PubMed 
    Article 

    Google Scholar 

  • Clinchy, M., Sheriff, M. J. & Zanette, L. Y. Predator-induced stress and the ecology of fear. Funct. Ecol. 27, 56–65 (2013).

    Article 

    Google Scholar 

  • Bolnick, D. I., Svanbäck, R., Araújo, M. S. & Persson, L. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc. Natl Acad. Sci. USA 104, 10075–10079 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Svanbäck, R. & Bolnick, D. I. Intraspecific competition drives increased resource use diversity within a natural population. Proc. R. Soc. B Biol. Sci. 274, 839–844 (2007).

    Article 

    Google Scholar 

  • Neudecker, S. Foraging patterns of Chaetodontid and Pomacanthis fishes at St. Croix (U.S. Virgin Islands). Proc. Fifth International Coral Reef Symposium. 415–414 (1985).

  • Lasker, H. Prey preferences and browsing pressure of the butterflyfish Chaetodon capistratus on Caribbean gorgonians. Mar. Ecol. Prog. Ser. 21, 213–220 (1985).

    Article 

    Google Scholar 

  • Cole, A. J., Pratchett, M. S. & Jones, G. P. Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish Fish. 9, 286–307 (2008).

    Article 

    Google Scholar 

  • Pratchett, M. S., Wilson, S. K., Berumen, M. L. & McCormick, M. I. Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23, 352–356 (2004).

    Article 

    Google Scholar 

  • Fishelson, L., Montgomery, W. L. & Myrberg, A. A. A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: teleostei) from the red sea. Science 229, 49–51 (1985).

    Article 

    Google Scholar 

  • Miyake, S., Ngugi, D. K. & Stingl, U. Phylogenetic diversity, distribution, and cophylogeny of giant bacteria (Epulopiscium) with their surgeonfish hosts in the Red Sea. Front. Microbiol. 7, 285 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Choat, J. H., Robbins, W. & Clements, K. The trophic status of herbivorous fishes on coral reefs II. Mar. Biol. 145, 445–454 (2004).

    Article 

    Google Scholar 

  • Elifantz, H., Horn, G., Ayon, M., Cohen, Y. & Minz, D. Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiol. Ecol. 85, 348–357 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Pujalte, M. J., Lucena, T., Ruvira, M. A., Arahal, D. R. & Macián, M. C. In The Prokaryotes: Alphaproteobacteria and Betaproteobacteria (Springer, 2014).

  • 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 

  • Sunagawa, S. et al. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512–521 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J. 8, 31–39 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Chiarello, M. et al. Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes. Proc. R. Soc. B Biol. Sci. 287, 20200642 (2020).

    Article 

    Google Scholar 

  • Sunagawa, S., Woodley, C. M. & Medina, M. Threatened corals provide underexplored microbial habitats. PLoS ONE 5, e9554 (2010).

  • Zhang, C. et al. Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME J. 10, 2235–2245 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Uren Webster, T. M. et al. Environmental plasticity and colonisation history in the Atlantic salmon microbiome: a translocation experiment. Mol. Ecol. 29, 886–898 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Fietz, K. et al. Mind the gut: genomic insights to population divergence and gut microbial composition of two marine keystone species. Microbiome 6, 82 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Smith, C. C., Snowberg, L. K., Caporaso, J. G., Knight, R. & Bolnick, D. I. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 9, 2515 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Uren Webster, T. M., Consuegra, S., Hitchings, M. & Garcia de Leaniz, C. Interpopulation variation in the Atlantic salmon microbiome reflects environmental and genetic diversity. Appl. Environ. Microbiol. 84, e00691-18 (2018).

  • Fiore, C. L., Labrie, M., Jarett, J. K. & Lesser, M. P. Transcriptional activity of the giant barrel sponge, Xestospongia muta holobiont: molecular evidence for metabolic interchange. Front. Microbiol. 6, 364 (2015).

  • 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).

  • 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Reverter, M., Sasal, P., Tapissier-Bontemps, N., Lecchini, D. & Suzuki, M. Characterisation of the gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems. FEMS Microbiol. Ecol. 93 (2017).

  • Parris, D. J., Brooker, R. M., Morgan, M. A., Dixson, D. L. & Stewart, F. J. Whole gut microbiome composition of damselfish and cardinalfish before and after reef settlement. PeerJ 4, e2412 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Reese, E. S. Coevolution of corals and coral feeding fishes of the family Chaetodontidae. In Proc. 3rd International Coral Reef Symposium, 267–274 (Rosenstiel School of Marine and Atmospheric Science, Miami, Florida., 1977).

  • Hammer, T. J. & Bowers, M. D. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1–14 (2015).

  • Kohl, K. D., Weiss, R. B., Cox, J., Dale, C. & Denise Dearing, M. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17, 1238–1246 (2014).

    PubMed 
    Article 

    Google Scholar 

  • Emslie, M. J., Pratchett, M. S., Cheal, A. J. & Osborne, K. Great Barrier Reef butterflyfish community structure: the role of shelf position and benthic community type. Coral Reefs 29, 705–715 (2010).

    Article 

    Google Scholar 

  • Noble, M. M., Pratchett, M. S., Coker, D. J., Cvitanovic, C. & Fulton, C. J. Foraging in corallivorous butterflyfish varies with wave exposure. Coral Reefs 33, 351–361 (2014).

    Article 

    Google Scholar 

  • Greb, L. et al. Ökologie und Sedimentologie eines rezenten Rampensystems an der Karibikküste von Panamá (Inst. für Geologie und Paläontologie, Stuttgart, 1996).

  • Aronson, R., Hilbun, N., Bianchi, T., Filley, T. & McKee, B. Land use, water quality, and the history of coral assemblages at Bocas del Toro, Panamá. Mar. Ecol. Prog. Ser. 504, 159–170 (2014).

    Article 

    Google Scholar 

  • Collin, R., D’Croz, L., Gondola, P. & Del Rosario, J. B. Climate and hydrological factors affecting variation in chlorophyll concentration and water clarity in the Bahia Almirante, Panama. Smithson. Contrib. Mar. Sci. 323–334 (2009).

  • D’Croz, L., Rosario, J. B.del. & Gondola, P. The effect of fresh water runoff on the distribution of dissolved inorganic nutrients and plankton in the Bocas del Toro Archipelago, Caribbean Panamá. Caribb. J. Sci. 41, 414–429 (2005).

    Google Scholar 

  • Seemann, J. et al. Assessing the ecological effects of human impacts on coral reefs in Bocas del Toro, Panama. Environ. Monit. Assess. 186, 1747–1763 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Guzmán, H. M., Barnes, P. A. G., Lovelock, C. E. & Feller, I. C. A site description of the CARICOMP mangrove, seagrass and coral reef sites in Bocas del Toro, Panamá. Caribb. J. Sci. 41, 430–440 (2005).

    Google Scholar 

  • Beijbom, O. et al. Towards automated annotation of benthic survey images: variability of human experts and operational modes of automation. PLoS ONE 10, e0130312 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Rocha, L. A., Jogan, J., Király, G., Feráková, V. & Bernhardt, K.-G. Chaetodon capistratus. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T165695A6094300.en (2010).

  • Froese, R. & D. P. E. FishBase. FishBase. 2019. www.fishbase.org (2020)

  • Smith, L. C. National Audubon Society Field Guide to Tropical Marine Fishes Caribbean, Gulf of Mexico, Florida, Bahamas, Bermuda (Alfred A. Knopf, 1997).

  • Nguyen, B. N. et al. Environmental DNA survey captures patterns of fish and invertebrate diversity across a tropical seascape. Sci. Rep. 10, 1–14 (2020).

    Article 
    CAS 

    Google Scholar 

  • Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).

    Article 

    Google Scholar 

  • Weber, L. et al. EMP 16S Illumina amplicon protocol. https://doi.org/10.17504/protocols.io.nuudeww (2018).

  • R Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria, 2019).

    Google Scholar 

  • Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10 (2011).

    Article 

    Google Scholar 

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

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wright, E. S. Using DECIPHER v2.0 to analyze big biological sequence data in R. R. J. 8, 352–359 (2016).

    Article 

    Google Scholar 

  • Schliep, K., Potts, A. J., Morrison, D. A. & Grimm, G. W. Intertwining phylogenetic trees and networks. Methods Ecol. Evol. 8, 1212–1220 (2017).

    Article 

    Google Scholar 

  • Weiss, S. et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5, 27 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Astudillo-García, C. et al. Evaluating the core microbiota in complex communities: a systematic investigation. Environ. Microbiol. 19, 1450–1462 (2017).

    PubMed 
    Article 

    Google Scholar 

  • Dufrêne, M. & Legendre, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).

    Google Scholar 

  • Roberts, D. W. labdsv: ordination and multivariate analysis for ecology. (2019).

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Leray, M. & Knowlton, N. Random sampling causes the low reproducibility of rare eukaryotic OTUs in Illumina COI metabarcoding. PeerJ 5, e3006 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Hill, M. O. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432 (1973).

    Article 

    Google Scholar 

  • Alberdi, A. & Gilbert, M. T. P. A guide to the application of Hill numbers to DNA‐based diversity analyses. Mol. Ecol. Resour. 19, 1755–0998.13014 (2019).

    Google Scholar 

  • Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).

    Article 

    Google Scholar 

  • Chiu, C. H. & Chao, A. Estimating and comparing microbial diversity in the presence of sequencing errors. PeerJ 2016, e1634 (2016).

    Article 
    CAS 

    Google Scholar 

  • Oksanen, J. et al. Community Ecology Package. Vienna R Found. Stat. Comput. https://doi.org/10.4135/9781412971874.n145 (2012).

  • Chen, J. et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28, 2106–2113 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576–1585 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jaccard, P. The distribution of the flora in the alpine zone.1. N. Phytol. 11, 37–50 (1912).

    Article 

    Google Scholar 

  • Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693 (2006).

    PubMed 
    Article 

    Google Scholar 

  • Bray, J. R. & Curtis, J. T. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27, 325–349 (1957).

    Article 

    Google Scholar 

  • Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).

    Google Scholar 

  • Anderson, M. J. & Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. 83, 557–574 (2013).

    Article 

    Google Scholar 

  • Martinez Arbizu, P. pairwiseAdonis: pairwise multilevel comparison using adonis. R package version 0.3. https://github.com/pmartinezarbizu/pairwiseAdonis (2019).

  • Roesch, L. F. W. et al. Pime: a package for discovery of novel differences among microbial communities. Mol. Ecol. Resour. 20, 415–428 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).

    Article 

    Google Scholar 

  • Klaus, J. S., Janse, I., Heikoop, J. M., Sanford, R. A. & Fouke, B. W. Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ. Microbiol. 9, 1291–1305 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ward, R. J. et al. Gastrointestinal Bacterial Symbionts: Reproductive Strategy and Community Structure. Thesis, Cornell Univ. (2009).

  • Séré, M. G. et al. Bacterial communities associated with Porites White Patch Syndrome (PWPS) on three Western Indian Ocean (WIO) coral reefs. PLoS ONE 8, e83746 (2013).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Moran, D., Turner, S. J. & Clements, K. D. Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microb. Ecol. 49, 590–597 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Mausz, M., Schmitz-Esser, S. & Steiner, G. Identification and comparative analysis of the endosymbionts of Loripes lacteus and Anodontia fragilis (Bivalvia: Lucinidae). (University of Vienna, 2008).

  • Bano, N., DeRae Smith, A., Bennett, W., Vasquez, L. & Hollibaugh, J. T. Dominance of mycoplasma in the guts of the long-jawed mudsucker, Gillichthys mirabilis, from five California salt marshes. Environ. Microbiol. 9, 2636–2641 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Frade, P. R., Roll, K., Bergauer, K. & Herndl, G. J. Archaeal and Bacterial Communities associated with the surface mucus of Caribbean corals differ in their degree of host specificity and community turnover over reefs. PLoS ONE 11, e0144702 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

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

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kimes, N. E. et al. The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline. Environ. Microbiol. 15, 2082–2094 (2013).

    PubMed 
    Article 

    Google Scholar 

  • Smriga, S., Sandin, S. A. & Azam, F. Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol. Ecol. 73, no–no (2010).

    Article 
    CAS 

    Google Scholar 

  • Zhang, X. et al. Effects of dietary supplementation of Ulva pertusa and non-starch polysaccharide enzymes on gut microbiota of Siganus canaliculatus. J. Oceanol. Limnol. 36, 438–449 (2018).

    CAS 
    Article 

    Google Scholar 

  • Klaus, J. S., Janse, I. & Fouke, B. W. Coral black band disease microbial communities and genotypic variability of the dominant cyanobacteria (CD1C11). Bull. Mar. Sci. 87, 795–821 (2011).

    Article 

    Google Scholar 

  • Lu, J., Santo Domingo, J. W., Hill, S. & Edge, T. A. Microbial diversity and host-specific sequences of Canada goose feces. Appl. Environ. Microbiol. 75, 5919–5926 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ueki, A., Goto, K., Ohtaki, Y., Kaku, N. & Ueki, K. Description of Anaerotignum aminivorans gen. Nov., sp. nov., a strictly anaerobic, amino-acid-decomposing bacterium isolated from a methanogenic reactor, and reclassification of Clostridium propionicum, Clostridium neopropionicum and Clostridium lactatifermentans as species of the genus Anaerotignum. Int. J. Syst. Evol. Microbiol. 67, 4146–4153 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bowman, K. S., Rainey, F. A. & Moe, W. M. Production of hydrogen by Clostridium species in the presence of chlorinated solvents. FEMS Microbiol. Lett. 290, 188–194 (2008).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Bueno de Mesquita, C. P., Sartwell, S. A., Schmidt, S. K. & Suding, K. N. Growing‐season length and soil microbes influence the performance of a generalist bunchgrass beyond its current range. Ecology 101, e03095 (2020).

  • Clever, F. et al. The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs. Dryad Datasets. https://doi.org/10.5061/dryad.m905qfv28 (2022).

  • Clever, F. & Scott, J. J. R code for reproducing the statistical analyses and figures of ‘The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs’. Commun. Biol. https://github.com/bocasbiome/web/ (2022).


  • Source: Ecology - nature.com

    Biogeographic implication of temperature-induced plant cell wall lignification

    Chemotaxis may assist marine heterotrophic bacterial diazotrophs to find microzones suitable for N2 fixation in the pelagic ocean