Abstract
Reef-building corals form complex relationships with a range of microorganisms including bacteria, archaea, fungi and the unicellular microalgae of the genus Symbiodinium, which together form the coral holobiont. These symbionts are known to have both beneficial and deleterious effects on their coral host, but little is known about what the governing factors of these relationships are, or the interactions that exist between the different members of the holobiont and their environment. Here we used 16S ribosomal RNA gene amplicon sequencing to investigate how archaeal and bacterial communities associated with the widespread scleractinian coral Seriatopora hystrix are influenced by extrinsic (reef habitat and geographic location) and intrinsic (host genotype and Symbiodinium subclade) factors. Bacteria dominate the microbiome of S. hystrix, with members of the Alphaproteobacteria, Gammaproteobacteria and Bacteriodetes being the most predominant in all samples. The richness and evenness of these communities varied between reef habitats, but there was no significant difference between distinct coral host lineages or corals hosting distinct Symbiodinium subclades. The coral microbiomes correlated to reef habitat (depth) and geographic location, with a negative correlation between Alpha- and Gammaproteobacteria, driven by the key members of both groups (Rhodobacteraceae and Hahellaceae, respectively), which showed significant differences between location and depth. This study suggests that the control of microbial communities associated with the scleractinian coral S. hystrix is driven primarily by external environmental conditions rather than by those directly associated with the coral holobiont.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Ainsworth TD, Hoegh-Guldberg O . (2009). Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aqua Biol 4: 289–296.
Anthony KRN, Fabricius KE . (2000). Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252: 221–253.
Apprill A, Marlow HQ, Martindale MQ, Rappe MS . (2009). The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3: 685–699.
Apprill A, Hughen K, Mincer T . (2013). Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ Microbiol 15: 2063–2072.
Baker AC . (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol S 34: 661–689.
Balser TC, McMahon KD, Bart D, Bronson D, Coyle DR, Craig N et al. (2006). Bridging the gap between micro- and macro-scale perspectives on the role of microbial communities in global change ecology. Plant Soil 289: 59–70.
Banin E, Israely T, Kushmaro A, Loya Y, Orr E, Rosenberg E . (2000). Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. Appl Environ Microbiol 66: 3031–3036.
Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK, Mincer T et al. (2013). The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas Bacteria. Appl Environ Microbiol 79: 4759–4762.
Becker PT, Gillan DC, Eeckhaut I . (2009). Characterization of the bacterial community associated with body wall lesions of Tripneustes gratilla (Echinoidea) using culture-independent methods. J Invertebr Pathol 100: 127–130.
Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA . (2007). Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73: 5642–5647.
Benlloch S, RodriguezValera F, MartinezMurcia AJ . (1995). Bacterial diversity in two coastal lagoons deduced from 16S rDNA PCR amplification and partial sequencing. FEMS Microbiol Ecol 18: 267–279.
Berga M, Szekely AJ, Langenheder S . (2012). Effects of disturbance intensity and frequency on bacterial community composition and function. PLoS One 7: e36959.
Berkelmans R, Oliver JK . (1999). Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18: 55–60.
Berkelmans R, De'ath G, Kininmonth S, Skirving WJ . (2004). A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23: 74–83.
Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N et al. (2010). Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5: e10871.
Bongaerts P, Riginos C, Hay KB, van Oppen MJH, Hoegh-Guldberg O, Dove S . (2011a). Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol Biol 11: 303.
Bongaerts P, Sampayo EM, Bridge TCL, Ridgway T, Vermeulen F, Englebert N et al. (2011b). Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Mar Ecol Prog Ser 439: 117–126.
Bourne D, Iida Y, Uthicke S, Smith-Keune C . (2008). Changes in coral-associated microbial communities during a bleaching event. ISME J 2: 350–363.
Bourne DG, Munn CB . (2005). Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7: 1162–1174.
Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW . (2012). Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9: 425–426.
Buckling A, Kassen R, Bell G, Rainey PB . (2000). Disturbance and diversity in experimental microcosms. Nature 408: 961–964.
Bythell JC, Barer MR, Cooney RP, Guest JR, O'Donnell AG, Pantos O et al. (2002). Histopathological methods for the investigation of microbial communities associated with disease lesions in reef corals. Lett Appl Microbiol 34: 359–364.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
Case RJ, Longford SR, Campbell AH, Low A, Tujula N, Steinberg PD et al. (2011). Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ Microbiol 13: 529–537.
Castillo I, Lodeiros C, Nunez M, Campos I . (2001). In vitro evaluation of antibacterial substances produced by bacteria isolated from different marine organisms. Rev Biol Trop 49: 1213–1221.
Ceh J, Raina J-B, Soo RM, van Keulen M, Bourne DG . (2012). Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef. PLoS One 7: e36920.
Chen C-P, Tseng C-H, Chen CA, Tang S-L . (2011). The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5: 728–740.
Cooney RP, Pantos O, Le Tissier MDA, Barer MR, O'Donnell AG, Bythell JC . (2002). Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 4: 401–413.
Cooper TF, Lai M, Ulstrup KE, Saunders SM, Flematti GR, Radford B et al. (2011). Symbiodinium genotypic and environmental controls on lipids in reef-building corals. PLoS One 6: e201434.
Crossland CJ . (1987). In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6: 35–42.
De'ath G, Fabricius K . (2010). Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20: 840–850.
Dennis PG, Guo K, Imelfort M, Jensen P, Tyson GW, Rabaey K . (2013). Spatial uniformity of microbial diversity in a continuous bioelectrochemical system. Bioresour Technol 129: 599–605.
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069–5072.
Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L et al. (2008). Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One 3: e1584.
Douglas AE . (1998). Host benefit and the evolution of specialization in symbiosis. Heredity 81: 599–603.
Ducklow H, Mitchell R . (1979). Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24: 715–725.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R . (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.
Fabricius KE, Logan M, Weeks S, Brodie J . (2014). The effects of river run-off on water clarity across the central Great Barrier Reef. Mar Pollut Bull 84: 191–200.
Fernandes N, Case RJ, Longford SR, Seyedsayamdost MR, Steinberg PD, Kjelleberg S et al. (2011). Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. PLoS One 6: e27387.
Ferrier-Pages C, Leclercq N, Jaubert J, Pelegri SP . (2000). Enhancement of pico- and nanoplankton growth by coral exudates. Aqua Micro Ecol 21: 203–209.
Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW . (2002). Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68: 2214–2228.
Furby KA, Apprill A, Cervino JM, Ossolinski JE, Hughen KA . (2014). Incidence of lesions on Fungiidae corals in the eastern Red Sea is related to water temperature and coastal pollution. Mar Env Res 98: 29–38.
Guppy R, Bythell JC . (2006). Environmental effects on bacterial diversity in the surface mucus layer of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328: 133–142.
Hansson L, Agis M, Maier C, Weinbauer MG . (2009). Community composition of bacteria associated with cold-water coral Madrepora oculata: within and between colony variability. Mar Ecol Prog Ser 397: 89–102.
Harland AD, Navarro JC, Davies PS, Fixter LM . (1993). Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 117: 113–117.
Hong M-J, Yu Y-T, Chen CA, Chiang P-W, Tang S-L . (2009). Influence of species specificity and other factors on bacteria associated with the coral Stylophora pistillata in Taiwan. Appl Environ Microbiol 75: 7797–7806.
Ikeda Y, Miyachi S . (1995). Carbon dioxide fixation by photosynthesis and calcification for a solitary coral, Fungia sp. Bulletin Inst Oceangra 14: 61–67.
Imai I, Fujimaru D, Nishigaki T, Kurosaki M, Sugita H . (2006). Algicidal bacteria isolated from the surface of seaweeds from the coast of Osaka Bay in the Seto Inland Sea, Japan. Afr J Mar Sci 28: 319–323.
Jessen C, Lizcano JFV, Bayer T, Roder C, Aranda M, Wild C et al. (2013). In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS One 8: e62091.
Jiang L, Patel SN . (2008). Community assembly in the presence of disturbance: a microcosm experiment. Ecology 89: 1931–1940.
Johnston IS, Rohwer F . (2007). Microbial landscapes on the outer tissue surfaces of the reef-building coral Porites compressa. Coral Reefs 26: 375–383.
Kellogg RB, Patton JS . (1983). Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp. Mar Biol 75: 137–149.
Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ . (2010). Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol 12: 541–556.
Klaus JS, Janse I, Heikoop JM, Sanford RA, Fouke BW . (2007). Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol 9: 1291–1305.
Koh EGL . (1997). Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23: 379–398.
Koren O, Rosenberg E . (2008). Bacteria associated with the bleached and cave coral Oculina patagonica. Microb Ecol 55: 523–529.
Kurahashi M, Yokota A . (2007). Endozoicomonas elysicola gen. nov., sp nov., a gamma-proteobacterium isolated from the sea slug Elysia ornata. Syst Appl Microbiol 30: 202–206.
Kvennefors ECE, Sampayo EM, Ridgway T, Barnes AC, Hoegh-Guldberg O . (2010). Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS One 5: e10401.
Kvennefors ECE, Sampayo E, Kerr C, Vieira G, Roff G, Barnes AC . (2012). Regulation of bacterial communities through antimicrobial activity by the coral holobiont. Microb Ecol 63: 605–618.
LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK . (2003). Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48: 2046–2054.
LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW . (2004). High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23: 596–603.
LaJeunesse TC . (2005). ‘Species’ radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22: 570–581.
LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO et al. (2010). Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37: 785–800.
Leggat W, Hoegh-Guldberg O, Dove S, Yellowlees D . (2007). Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef-building corals. J Phycol 43: 1010–1021.
Lema KA, Willis BL, Bourne DG . (2012). Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78: 3136–3144.
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG . (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305: 997–1000.
Lesser MP, Falcon LI, Rodriguez-Roman A, Enriquez S, Hoegh-Guldberg O, Iglesias-Prieto R . (2007). Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346: 143–152.
Lins-de-Barros MM, Vieira RP, Cardoso AM, Monteiro VA, Turque AS, Silveira CB et al. (2010). Archaea, bacteria, and algal plastids associated with the reef-building corals Siderastrea stellata and Mussismilia hispida from Búzios, South Atlantic Ocean, Brazil. Microb Ecol 59: 523–532.
Littman R, Willis BL, Bourne DG . (2011). Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Rep 3: 651–660.
Littman RA, Willis BL, Bourne DG . (2009a). Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389: 45–59.
Littman RA, Willis BL, Pfeffer C, Bourne DG . (2009b). Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68: 152–163.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhu kumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371.
Meikle P, Richards GN, Yellowlees D . (1988). Structural investigations on the mucus from six species of coral. Mar Biol 99: 187–193.
Mouchka ME, Hewson I, Harvell CD . (2010). Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662–674.
Muscatine L, Porter JW . (1977). Coral Reefs: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: 454–460.
Nelson CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F et al. (2013). Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7: 962–979.
Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H . (2003). Seasonal changes in the content and composition of lipids in the coral Goniastrea aspera. Coral Reefs 22: 83–85.
Olson ND, Ainsworth TD, Gates RD, Takabayashi M . (2009). Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J Exp Mar Biol Ecol 371: 140–146.
Paul JH, DeFlaun MF, Jeffery WH . (1986). Elevated levels of microbial activity in the coral surface monolayer. Mar Ecol Prog Ser 33: 29–40.
Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O et al. (2012). A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J 6: 1314–1324.
Peters EC . (1984). A survey of cellular reactions to environmental-stress and disease in Caribbean scleractinian corals. Helgolander Meeresuntersuchungen 37: 113–137.
Raina J-B, Dinsdale EA, Willis BL, Bourne DG . (2010). Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18: 101–108.
Richardson LL, Goldberg WM, Carlton RG, Halas JC . (1998). Coral disease outbreak in the Florida keys: plague type II. Rev Biol Trop 46: 187–198.
Ritchie KB, Smith GW . (1995a). Preferential carbon utilization by surface bacterial communities from water mass, normal, and white-band diseased Acropora cervicornis. Mol Mar Biol Biotech 4: 345–352.
Ritchie KB, Smith GW . (1995b). Carbon-source utilization patterns of coral-associated marine heterotrophs. J Mar Biotechnol 3: 105–107.
Ritchie KB, Smith GW . (2004). Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral Health and Disease. Springer-Verlag: Berlin, Germany, pp 259–263.
Ritchie KB . (2006). Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1–14.
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N . (2001). Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20: 85–91.
Rohwer F, Seguritan V, Azam F, Knowlton N . (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1–10.
Rypien KL, Ward JR, Azam F . (2010). Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12: 28–39.
Santavy DL . (1995). The diversity of microorganisms associated with marine invertebrates and their roles in the maintenance of ecosystems. In: Allsopp D, Colwell RR, Hawksworth DL eds Microbial Diversity and Ecosystem Function. CAB International: Wallingford, WI, USA, pp 211–229.
Santavy DL, Peters EC . (1997). Microbial pests: Coral disease in the western Atlantic. Proc 8th Int Coral Reef Symp 1: 607–612.
Santiago-Vazquez LZ, Brueck TB, Brueck WM, Duque-Alarcon AP, McCarthy PJ, Kerr RG . (2007). The diversity of the bacterial communities associated with the azooxanthellate hexacoral Cirrhipathes lutkeni. ISME J 1: 654–659.
Schäfer H, Bernard L, Courties C, Lebaron P, Servais P, Pukall R et al. (2001). Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. FEMS Microbiol Ecol 34: 243–253.
Schöttner S, Wild C, Hoffmann F, Boetius A, Ramette A . (2012). Spatial scales of bacterial diversity in cold-water coral reef ecosystems. PLoS One 7: e32093.
Schuett C, Doepke H, Grathoff A, Gedde M . (2007). Bacterial aggregates in the tentacles of the sea anemone Metridium senile. Helgoland Mar Res 61: 211–216.
Sekar R, Kaczmarsky LT, Richardson LL . (2009). Effect of freezing on PCR amplification of 16S rRNA genes from microbes associated with black band disease of corals. Appl Environ Microbiol 75: 2581–2584.
Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ . (2010). Bacterial acquisition in juveniles of several broadcast spawning coral species. PLoS One 5: e10898.
Sharp KH, Distel D, Paul VJ . (2012). Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J 6: 790–801.
Shashar N, Cohen Y, Loya Y, Sar N . (1994). Nitrogen-fixation (acetylene-reduction) in stony corals: evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111: 259–264.
Siboni N, Ben-Dov E, Sivan A, Kushmaro A . (2008). Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10: 2979–2990.
Siboni N, Ben-Dov E, Sivan A, Kushmaro A . (2012). Geographic specific coral-associated ammonia-oxidizing Archaea in the Northern Gulf of Eilat (Red Sea). Microb Ecol 64: 18–24.
Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC . (2011). Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422: 63–75.
Simpson EH . (1949). Measurement of diversity. Nature 163: 688–688.
Sorokin YI . (1973). Trophic role of bacteria in ecosystem of coral reef. Nature 242: 415–417.
Speck MD, Donachie SP . (2012). Widespread Oceanospirillaceae bacteria in Porites spp. J Mar Biol 2012: 7.
Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA . (2008a). Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27: 763–772.
Stat M, Morris E, Gates RD . (2008b). Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105: 9256–9261.
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al. (2009). Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3: 512–521.
Sunagawa S, Woodley CM, Medina M . (2010). Threatened corals provide underexplored microbial habitats. PLoS One 5: e9554.
Tremblay P, Weinbauer MG, Rottier C, Guerardel Y, Nozais C, Ferrier-Pages C . (2011). Mucus composition and bacterial communities associated with the tissue and skeleton of three scleractinian corals maintained under culture conditions. J Mar Biol Assoc UK 91: 649–657.
Veron JEN, Pichon M . (1976) Marine Science Monograph Series 1: Scleractinia of Eastern Australia, Part 1. Families Thamnasteriidae, Astrocoeniidae, and Pocilloporidae. Australian Institute of Marine Science: Townsville, QLD, Australia.
Veron JEN . (2000) Corals of the World vol. 1–3. Australian Institute of Marine Science: Townsville, QLD, Australia.
Wegley L, Yu YN, Breitbart M, Casas V, Kline DI, Rohwer F . (2004). Coral-associated archaea. Mar Ecol Prog Ser 273: 89–96.
Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F . (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707–2719.
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB . (2004a). Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428: 66–70.
Wild C, Rasheed M, Werner U, Franke U, Johnstone R, Huettel M . (2004b). Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267: 159–171.
Wild C, Naumann M, Niggl W, Haas A . (2010a). Carbohydrate composition of mucus released by scleractinian warm- and cold-water reef corals. Aqua Biol 10: 41–45.
Wild C, Niggl W, Naumann MS, Haas AF . (2010b). Organic matter release by Red Sea coral reef organisms-potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411: 61–71.
Williams WM, Viner AB, Broughton WJ . (1987). Nitrogen-fixation (acetylene-reduction) associated with the living coral Acropora variabilis. Mar Biol 94: 531–535.
Yakimov MM, Cappello S, Crisafi E, Tursi A, Savini A, Corselli C et al. (2006). Phylogenetic survey of metabolically active microbial communities associated with the deep-sea coral Lophelia pertusa from the Apulian plateau, Central Mediterranean Sea. Deep-Sea Res Pt I 53: 62–75.
Yang CS, Chen MH, Arun AB, Chen CA, Wang JT, Chen WM . (2010). Endozoicomonas montiporae sp nov., isolated from the encrusting pore coral Montipora aequituberculata. Int J Syst Evol Microbiol 60: 1158–1162.
Acknowledgements
This study was conducted as part of the ‘Catlin Seaview Survey’ funded by Catlin Group Limited, with support from the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies and the Global Change Institute. GWT is supported by an ARC Queen Elizabeth II fellowship (DP1093175).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Rights and permissions
About this article
Cite this article
Pantos, O., Bongaerts, P., Dennis, P. et al. Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9, 1916–1927 (2015). https://doi.org/10.1038/ismej.2015.3
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2015.3
This article is cited by
-
Microbiome changes in Sinularia spp. soft corals relative to health status
Marine Biology (2024)
-
Diversity of the Pacific Ocean coral reef microbiome
Nature Communications (2023)
-
Differential responses of bacterial communities in coral tissue and mucus to bleaching
Coral Reefs (2022)
-
Shifts in marine invertebrate bacterial assemblages associated with tissue necrosis during a heat wave
Coral Reefs (2021)
-
Antagonism between coral pathogen Vibrio coralliilyticus and other bacteria in the gastric cavity of scleractinian coral Galaxea fascicularis
Science China Earth Sciences (2020)
