Reef-Building Corals as a Tool for Climate Change Research in the Genomics Era

  • Filipa Godoy-Vitorino
  • Carlos Toledo-Hernandez
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)


Coral reef ecosystems are among the most biodiverse habitats in the marine realm. They not only contribute with a plethora of ecosystem services, but they also are beneficial to humankind via nurturing marine fisheries and sustaining recreational activities. We will discuss the biology of coral reefs and their ecophysiology including the complex bacterial microbiota associated with them.


Scleractinian corals Coral microbiome Holobiont Climate change Next-generation sequencing 


  1. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methe B, Schloss PD, Gevers D, Mitreva M, Huttenhower C (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8(6):e1002358. Scholar
  2. Agostini S, Suzuki Y, Casareto BE, Nakano Y, Hidaka M, Badrun N (2009) Coral symbiotic complex: hypothesis through vitamin B12 for a new evaluation. Galaxea J Coral Reef Stud 11:1–11CrossRefGoogle Scholar
  3. Ainsworth TD, Krause L, Bridge T, Torda G, Raina J, Zakrzewski M, Gates R, Padilla-Gamiño C, Spalding H, Smith C, Woolsey E, Bourne D, Bongaerts P, Hoegh-Guldberg O, Leggat W (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274CrossRefGoogle Scholar
  4. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the early Archaean era of Australia. Nature 441(7094):714–718. Scholar
  5. Amend AS, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 6(7):1291–1301. Scholar
  6. Antonius A (1973) New observations on coral destruction in reefs. Abs Assoc Isl Mar Lab Caribb 10:3Google Scholar
  7. Baker AC, Glynns PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  8. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, Mauceli E, Berger B, Mesirov JP, Lander ES (2002) ARACHNE: a whole-genome shotgun assembler. Genome Res 12(1):177–189. Scholar
  9. Bond-Lamberty B, Bolton H, Fansler S, Heredia-Langner A, Liu C, McCue LA, Smith J, Bailey V (2016) Soil respiration and bacterial structure and function after 17 years of a reciprocal soil transplant experiment. PLoS One 11(3):e0150599. Scholar
  10. Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340CrossRefPubMedGoogle Scholar
  11. Bridge TC, Hoey AS, Campbell SJ, Muttaqin E, Rudi E, Fadli N, Baird AH (2013) Depth-dependent mortality of reef corals following a severe bleaching event: implications for thermal refuges and population recovery. F1000Res 2:187. Scholar
  12. Brodie EL, Desantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL, Hazen TC, Richardson PM, Herman DJ, Tokunaga TK, Wan JM, Firestone MK (2006) Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72(9):6288–6298CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brück TB, Brück WM, Santiago-Vázquez LZ, McCarthy PJ, Kerr RG (2007) Diversity of the bacterial communities associated with the azooxanthellate deep water octocorals Leptogorgia minimata, Iciligorgia schrammi, and Swiftia exertia. Mar Biotechnol (NY) 9(5):561–576CrossRefGoogle Scholar
  14. Bruno JF, Selig ER (2007) regional decline of coral cover in the indo-pacific: timing, extent, and subregional comparisons. PLoS One 2(8):e711CrossRefPubMedPubMedCentralGoogle Scholar
  15. Buchsmaum Pearse V, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in Coral Calcification. Biol Bull 141(2):350–363CrossRefGoogle Scholar
  16. Budd AF, Romano SL, Smith ND, Barbeitos MS (2010) Rethinking the phylogeny of scleractinian corals: a review of morphological and molecular data. Integr Comp Biol 50:411–427CrossRefPubMedGoogle Scholar
  17. Cai L, Tian RM, Zhou G, Tong H, Wong YH, Zhang W, Chui APY, Xie JY, Qiu JW, Ang PO, Liu S, Huang H, Qian PY (2018) Exploring coral microbiome assemblages in the South China Sea. Sci Rep 8(1):2428. Scholar
  18. Cairns SD (1999) Species richness of recent Scleractinia. Atoll Res Bull 459:1–46. Scholar
  19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. Scholar
  20. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522. Scholar
  21. Claesson MJ, Wang Q, O’Sullivan O, Greene-Diniz R, Cole JR, Ross RP, O’Toole PW (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38(22):e200. Scholar
  22. Closek CJ, Sunagawa S, DeSalvo MK, Piceno YM, DeSantis TZ, Brodie EL, Weber MX, Voolstra CR, Andersen GL, Medina M (2014) Coral transcriptome and bacterial community profiles reveal distinct Yellow Band Disease states in Orbicella faveolata. ISME J 8(12):2411–2422. Scholar
  23. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33(Database issue):D294–D296CrossRefPubMedGoogle Scholar
  24. Crossland CJ, Hatcher BG, Smith SV (1991) Role of coral reefs in global ocean production. Coral Reefs 10:55–64CrossRefGoogle Scholar
  25. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan R, Cote IM (2012) Evaluation life-history strategies of reef corals from species traits. Ecol Lett 15(12):1378–1386. Scholar
  26. de Voogd NJ, Cleary DF, Polonia AR, Gomes NC (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West Java, Indonesia. FEMS Microbiol Ecol 91(4).
  27. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  28. Desriac F, Jegou C, Balnois E, Brillet B, Le Chevalier P, Fleury Y (2013) Antimicrobial peptides from marine proteobacteria. Mar Drugs 11(10):3632–3660. Scholar
  29. Eisen JA (2007) Environmental shotgun sequencing: its potential and challenges for studying the hidden world of microbes. PLoS Biol 5(3):e82. Scholar
  30. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4(6):457–469. Scholar
  31. Eren AM, Esen OC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3:e1319. Scholar
  32. Falkowski PG, Dubinsky Z, Nuscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. Bioscience 34(11):705–709CrossRefGoogle Scholar
  33. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA 109(27):E1878–E1887. Scholar
  34. Fernando SC, Wang J, Sparling K, Garcia GD, Francini-Filho RB, de Moura RL, Paranhos R, Thompson FL, Thompson JR (2015) Microbiota of the major South Atlantic reef building coral Mussismilia. Microb Ecol 69(2):267–280. Scholar
  35. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(Database issue):D211–D222. Scholar
  36. Fitt WK, McFarlland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  37. Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW, Delong EF (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105(10):3805–3810. Scholar
  38. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson R (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960CrossRefGoogle Scholar
  39. Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interaction and control by carbonate chemistry. Am Zool 39:160–183CrossRefGoogle Scholar
  40. Gilbert JA, Meyer F, Jansson J, Gordon J, Pace N, Tiedje J, Ley R, Fierer N, Field D, Kyrpides N, Glockner FO, Klenk HP, Wommack KE, Glass E, Docherty K, Gallery R, Stevens R, Knight R (2010) The Earth Microbiome Project: meeting report of the “1 EMP meeting on sample selection and acquisition” at Argonne National Laboratory October 6 2010. Stand Genomic Sci 3(3):249–253. Scholar
  41. Godoy-Vitorino F, Ruiz-Diaz CP, Rivera-Seda A, Ramirez-Lugo JS, Toledo-Hernandez C (2017) The microbial biosphere of the coral Acropora cervicornis in Northeastern Puerto Rico. PeerJ 5:e3717. Scholar
  42. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440(7088):1186–1189. Scholar
  43. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5(10):R245–R249CrossRefPubMedGoogle Scholar
  44. Hartmann AC, Petras D, Quinn RA, Protsyuk I, Archer FI, Ransome E, Williams GJ, Bailey BA, Vermeij MJA, Alexandrov T, Dorrestein PC, Rohwer FL (2017) Meta-mass shift chemical profiling of metabolomes from coral reefs. Proc Natl Acad Sci USA 114(44):11685–11690. Scholar
  45. Hernandez-Zulueta J, Araya R, Vargas-Ponce O, Diaz-Perez L, Rodriguez-Troncoso AP, Ceh J, Rios-Jara E, Rodriguez-Zaragoza FA (2016) First deep screening of bacterial assemblages associated with corals of the Tropical Eastern Pacific. FEMS Microbiol Ecol 92(12).
  46. Higa T, Tanaka J, Ohtani II, Musman M, Roy MC, Kuroda I (2001) Bioactive compounds from coral reef invertebrates. Pure Appl Chem 73:589–593CrossRefGoogle Scholar
  47. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328(5985):1523–1528. Scholar
  48. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318(5857):1737–1742. Scholar
  49. Houbreque F, Ferrier-Pages C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84(1):1–17Google Scholar
  50. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF (2016) A new view of the tree of life. Nat Microbiol 1:16048. Scholar
  51. Kappler A, Pasquero C, Konhauser KO, Newman DK (2005) Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria. Geology 33(11):865–868. Scholar
  52. 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(2):541–556. Scholar
  53. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98(10):5419–5425. Scholar
  54. Knowlton N, Brainard R, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral reef biodiversity. In: McIntyre a life in the World’s oceans: diversity, distribution, and abundance. Wiley-Blackwell, Oxford, pp 65–79CrossRefGoogle Scholar
  55. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72(8):5254–5259. Scholar
  56. Laval B, Cady SL, Pollack JC, McKay CP, Bird JS, Grotzinger JP, Ford DC, Bohm HR (2000) Modern freshwater microbialite analogues for ancient dendritic reef structures. Nature 407(6804):626–629. Scholar
  57. Lederberg J, McCray AT (2001) “Ome Sweet Omics”—a genealogical treasury of words. Scientist 15:8Google Scholar
  58. Leite DCA, Salles JF, Calderon EN, van Elsas JD, Peixoto RS (2018) Specific plasmid patterns and high rates of bacterial co-occurrence within the coral holobiont. Ecol Evol 8(3):1818–1832CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305(5686):997–1000. Scholar
  60. Levitus S, Antonov JI, Boyer TP, Locarnini RA, Garcia HE, Mishonov AV (2009) Global ocean heat content 1955–2008 in light of recently revealed instrumentation problems. Geophys Res Lett 36:L07608. Scholar
  61. Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72(5):3685–3695CrossRefPubMedPubMedCentralGoogle Scholar
  62. Liu Z, DeSantis TZ, Andersen GL, Knight R (2008) Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res 36(18):e120. Scholar
  63. Lough JM (2010) Climate records from corals. WIREs Clim Change 1.
  64. Marcelino VR, Morrow KM, van Oppen MJH, Bourne DG, Verbruggen H (2017) Diversity and stability of coral endolithic microbial communities at a naturally high pCO2 reef. Mol Ecol 26(19):5344–5357. Scholar
  65. McCauley EP, Haltli B, Correa H, Kerr RG (2016) Spatial and temporal investigation of the microbiome of the Caribbean octocoral Erythropodium caribaeorum. FEMS Microbiol Ecol 92(9).
  66. McDonald D, Price MN, Goodrich J, Nawrocki EP, Desantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2011) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J.
  67. Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7:11257. Scholar
  68. Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233CrossRefGoogle Scholar
  69. Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP, Friend CR (1996) Evidence for life on Earth before 3,800 million years ago. Nature 384(6604):55–59CrossRefPubMedGoogle Scholar
  70. Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D (2005) Stable isotopes (delta13C and delta15N) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102(5):1525–1530. Scholar
  71. Namiki T, Hachiya T, Tanaka H, Sakakibara Y (2012) MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res 40(20):e155. Scholar
  72. Nelson CE, Goldberg SJ, Wegley Kelly L, Haas AF, Smith JE, Rohwer F, Carlson CA (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7(5):962–979. Scholar
  73. Novais RC, Thorstenson YR (2011) The evolution of Pyrosequencing(R) for microbiology: from genes to genomes. J Microbiol Methods 86(1):1–7. Scholar
  74. Ohde S, Van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65:559–576Google Scholar
  75. Okubo N, Mezaki T, Nozawa Y, Nakano Y, Lien YT, Fukami H, Hayward DC, Ball EE (2013) Comparative embryology of eleven species of stony corals (Scleractinia). PLoS One 8(12):e84115. Scholar
  76. Olson JM (2006) Photosynthesis in the Archean era. Photosynth Res 88(2):109–117CrossRefPubMedGoogle Scholar
  77. Pereira LB, Palermo BRZ, Carlos C, Ottoboni LMM (2017) Diversity and antimicrobial activity of bacteria isolated from different Brazilian coral species. FEMS Microbiol Lett 364(16).
  78. Pootakham W, Mhuantong W, Yoocha T, Putchim L, Sonthirod C, Naktang C, Thongtham N, Tangphatsornruang S (2017) High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci Rep 7(1):2774. Scholar
  79. Prescott SL, Larcombe DL, Logan AC, West C, Burks W, Caraballo L, Levin M, Etten EV, Horwitz P, Kozyrskyj A, Campbell DE (2017) The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J 10(1):29. Scholar
  80. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35(21):7188–7196. Scholar
  81. Putria DA, Radja OK, Pringgenies D (2015) Effectiveness of marine fungal symbiont isolated from soft coral Sinularia sp. from Panjang Island as antifungal. Procedia Environ Sci 23:351–357CrossRefGoogle Scholar
  82. Rappé MS, Kemp PF, Giovannoni SJ (1997) Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina. Limnol Oceanogr 42:811–826CrossRefGoogle Scholar
  83. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  84. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499(7459):431–437. Scholar
  85. Rocha J, Peixe L, Gomes-Newton CM, Calado R (2011) Cnidarians as a source of new marine bioactive compounds—an overview of the last decade and future steps for bioprospecting. Mar Drugs 9:1860–1886CrossRefPubMedPubMedCentralGoogle Scholar
  86. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 2243:1–10CrossRefGoogle Scholar
  87. Rosenberg E, Zilber-Rosenberg I (2013) Microbiotas are transmitted between holobiont generations. In: The hologenome concept: human, animal and plant microbiota. Springer, Cham. Scholar
  88. Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. MBio 7(2):e01395. Scholar
  89. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. Scholar
  90. Ruiz-Diaz CP, Toledo-Hernández C, Mercado-Molina AE, Sabat AM (2016) Scraping and extirpating: two strategies to induce recovery of diseased Gorgonia ventalina sea fans. Mar Ecol 4:e1531Google Scholar
  91. Santer BD, Taylor KE, Wigley TML, Johns TC, Jones PD, Karoly DJ, Mitchell JFB, Oort AH, Penner JE, Ramaswamy V, Schwarzkopf MD, Stouffer RJ, Tett S (1996) A search for human influences on the thermal structure of the atmosphere. Nature 382:39–46CrossRefGoogle Scholar
  92. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. Scholar
  93. Schopf JW (2011) The paleobiological record of photosynthesis. Photosynth Res 107(1):87–101. Scholar
  94. Schweinsberg M, Weiss LC, Striewski S, Tollrian R, Lampert KP (2015) More than one genotype: how common is intracolonial genetic variability in scleractinian corals? Mol Ecol 24:2673–2685CrossRefPubMedGoogle Scholar
  95. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C (2012) Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 9(8):811–814. Scholar
  96. Selengut JD, Haft DH, Davidsen T, Ganapathy A, Gwinn-Giglio M, Nelson WC, Richter AR, White O (2007) TIGRFAMs and genome properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res 35(Database issue):D260–D264. Scholar
  97. 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(4):790–801. Scholar
  98. Sheppard C, Dixon DJ, Gourlay M, Sheppard A, Payet R (2005) Coral mortality increases wave energy reaching shores protected by reef flats: examples from the Seychelles. Estuar Coast Shelf Sci 64:223–234CrossRefGoogle Scholar
  99. Sheridan C, Baele JM, Kushmaro A, Frejaville Y, Eeckhaut I (2014) Terrestrial runoff influences white syndrome prevalence in SW Madagascar. Mar Environ Res 101:44–51. Scholar
  100. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fukie M, Fujiwara M, Koyangi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–324CrossRefPubMedGoogle Scholar
  101. Staley C, Kaiser T, Gidley ML, Enochs IC, Jones PR, Goodwin KD, Sinigalliano CD, Sadowsky MJ, Chun CL (2017) Differential impacts of land-based sources of pollution on the microbiota of Southeast Florida coral reefs. Appl Environ Microbiol 83(10).
  102. Sun W, Anbuchezhian R, Li Z (2016) Association of coral-microbes, and the ecological roles of microbial symbionts in corals. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. Springer, Switzerland, pp 347–357CrossRefGoogle Scholar
  103. Sutherland KP, Shaban S, Joyner JL, Porter JW, Lipp EK (2011) Human pathogen shown to cause disease in the threatened elkhorn coral Acropora palmata. PLoS One 6(8):e23468. Scholar
  104. Suzuki MT, Rappé MS, Haimberger ZW, Winfield H, Adair N, Ströbel J, Giovannoni SJ (1997) Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample. Appl Environ Microbiol 63(3):983–989PubMedPubMedCentralGoogle Scholar
  105. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278(5338):631–637CrossRefPubMedGoogle Scholar
  106. Thompson JR, Rivera HE, Closek CJ, Medina M (2014) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4:176. Scholar
  107. Toledo-Hernández C, Ruiz-Diaz CP (2014) The immune responses of the coral. ISJ 11:319–328Google Scholar
  108. Trindade-Silva AE, Lim-Fong GE, Sharp KH, Haygood MG (2010) Bryostatins: biological context and biotechnological prospects. Curr Opin Biotechnol 21(6):834–842. Scholar
  109. Tuomi J, Vuorisalo T (1989) What are the units of selection in modular organisms? Oikos 54:227–233CrossRefGoogle Scholar
  110. Webster NS, Reusch TBH (2017) Microbial contributions to the persistence of coral reefs. ISME J 11:2167–2174CrossRefPubMedPubMedCentralGoogle Scholar
  111. Wilde SA, Valley JW, Peck WH, Graham CM (2001) Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago. Nature 409(6817):175–178CrossRefPubMedGoogle Scholar
  112. Wilkinson C (2004) Status of the coral reefs of the world, vol 1+2. Global Coral Reef Monitoring Network and Australian Institute of Marine Science, Townsville, QLDGoogle Scholar
  113. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236CrossRefPubMedGoogle Scholar
  114. Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95(12):6854–6859CrossRefPubMedGoogle Scholar
  115. Wood R (1998) The ecological evolution of reefs. Annu Rev Ecol Syst 29:179–206CrossRefGoogle Scholar
  116. Wood DE, Salzberg SL (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15(3):R46. Scholar
  117. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, Cordum H, Van Brunt A, Kim K, Fulton RS, Fulton LA, Clifton SW, Wilson RK, Knight RD, Gordon JI (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5(7):e156. Scholar
  118. Yang B, Wang Y, Qian PY (2016) Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformatics 17:135. Scholar
  119. Yokouchi H, Fukuoka Y, Mukoyama D, Calugay R, Takeyama H, Matsunaga T (2006) Whole-metagenome amplification of a microbial community associated with scleractinian coral by multiple displacement amplification using phi29 polymerase. Environ Microbiol 8(7):1155–1163. Scholar
  120. Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105(2):629–640. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Filipa Godoy-Vitorino
    • 1
  • Carlos Toledo-Hernandez
    • 2
  1. 1.Department of Microbiology and Medical ZoologyUniversity of Puerto-Rico-School of Medicine, Medical Sciences CampusSan JuanUSA
  2. 2.Sociedad Ambiente MarinoSan JuanUSA

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