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Global Networks of Symbiodinium-Bacteria Within the Coral Holobiont

  • Rachele Bernasconi
  • Michael Stat
  • Annette Koenders
  • Megan J. Huggett
Host Microbe Interactions

Abstract

Scleractinian corals form the framework of coral reefs and host abundant and diverse microbial communities that are fundamental to their success. A very limited number of studies have examined the co-occurrence of multiple partners within the coral ‘holobiont’ and their pattern of specificity over different geographical scales. In this study, we explored two molecular sequence datasets representing associations between corals and dinoflagellates in the genus Symbiodinium and between corals and bacteria, across the globe. Through a network theory approach, we characterised patterns of co-occurrences between bacteria and Symbiodinium with 13 coral genera across six water basins. The majority of the bacteria-Symbiodinium co-occurrences were specific to either a coral genus or water basin, emphasising both coral host and environment as important factors driving the diversity of coral assemblages. Yet, results also identified bacteria and Symbiodinium that were shared by multiple coral genera across several water basins. The analyses indicate that shared co-occurrences are independent of the phylogenetic and biogeographic relationship of coral hosts.

Keywords

16S rRNA Bacteria Co-occurrences Coral reefs ITS2 Network analysis Symbiodinium 

Notes

Acknowledgments

We would like to thank Prof. Jordi Bascompte’s lab members for their useful guidance and advice in the selection of the appropriate methods for the exploration of the data. We also thank the three anonymous reviewers for their feedback.

Supplementary material

248_2018_1255_MOESM1_ESM.xlsx (1.1 mb)
Data S1 Heatmap representing all bacteria OTU-Symbiodinium type co-occurrences that were identified across the coral genera network. Each cell in the spreadsheet represents a node in the network shown in Fig. S1. Nodes are characterised by an degree of between zero (co-occurrences not detected across any of the coral genera) and six (co-occurrences shared by six coral genera) (XLSX 1174 kb)
248_2018_1255_MOESM2_ESM.xlsx (1.1 mb)
Data S2 Heatmap representing all the bacteria OTU-Symbiodinium type co-occurrences that were identified across six water basins. Each cell in the spreadsheet represents a node in the network shown in Fig. S2. Nodes are characterised by a degree of between zero (co-occurrences not detected across any of the water basins examined) and three (co-occurrences that were shared by three water basins) (XLSX 1138 kb)
248_2018_1255_MOESM3_ESM.xlsx (1.1 mb)
Data S3 Heatmap representing all bacteria OTUs-Symbiodinium types co-occurrences that were identified across 13 coral genera and six water basins. Each cell in the spreadsheet represents a node in the network shown in Fig. S3. Nodes are characterised by a degree of between zero (co-occurrences not detected across any of the coral genera and water basins examined) and nine. No degree one is detected as each bacteria-Symbiodinium co-occurrence is located in at least one coral genus and one water basin (degree two) (XLSX 1148 kb)
248_2018_1255_MOESM4_ESM.docx (1.4 mb)
Fig. S1 Bacteria-Symbiodinium co-occurrences identified across 13 coral genera. a) Network of co-occurrences with nodes representing b) bacteria-Symbiodinium co-occurrences (degree one to six) and coral genera. Nodes of degree values above two are show in detail in Fig. 1 (DOCX 1439 kb)
248_2018_1255_MOESM5_ESM.docx (1.2 mb)
Fig. S2 Bacteria-Symbiodinium co-occurrences identified across six water basins. a) Network of co-occurrences with nodes representing b) bacteria-Symbiodinium co-occurrences (degree one to three) and water basins. Nodes of degree values above two are shown in detail in Fig.  3 (DOCX 1194 kb)
248_2018_1255_MOESM6_ESM.docx (1.8 mb)
Fig. S3 Bacteria-Symbiodinium co-occurrences identified across 13 coral genera and six water basins. a) Network of co-occurrences with nodes representing b) bacteria-Symbiodinium co-occurrences (degree two to nine) and the water basins/coral genera. Nodes of degree values above six are shown in detail in Fig. 5 (DOCX 1803 kb)

References

  1. 1.
    Rosenberg E, Koren O, Reshef L et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362.  https://doi.org/10.1038/nrmicro1635 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Stat M, Baker AC, Bourne DG et al (2012) Molecular delineation of species in the coral holobiont. Adv Mar Biol 63:1–66CrossRefPubMedCentralGoogle Scholar
  3. 3.
    Sharp KH, Ritchie KB (2012) Multi-partner interactions in corals in the face of climate change. Biol Bull 223:66–77CrossRefPubMedCentralGoogle Scholar
  4. 4.
    Fournier A (2013) The story of symbiosis with zooxanthellae, or how they enable their host to thrive in a nutrient poor environment. Masters Bioscience Review - Ecole Normale Supérieure de Lyon :1–8Google Scholar
  5. 5.
    Herndl GJ, Velimirov B (1986) Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora cespitosa. Mar Biol 90(3):363–369.  https://doi.org/10.1007/BF00428560 CrossRefGoogle Scholar
  6. 6.
    Falkowski PG, Gan R, Wyman K (1985) Growth-irradiance relationships in phytoplankton. Limnol Oceanogr 30:311–321CrossRefGoogle Scholar
  7. 7.
    Muller-Parker G, D’Elia CF (1997) Interactions between corals and their symbiotic algae. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 96–113CrossRefGoogle Scholar
  8. 8.
    Braga RM, Dourado MN, Araújo WL (2016) Microbial interactions: ecology in a molecular perspective. Braz J Microbiol 47:86–98.  https://doi.org/10.1016/j.bjm.2016.10.005 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Fabina NS, Putnam HM, Franklin EC et al (2012) Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks. PLoS One 7:1–9.  https://doi.org/10.1371/journal.pone.0044970 CrossRefGoogle Scholar
  10. 10.
    Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD (2013) Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses. Glob Chang Biol 19:3306–3316.  https://doi.org/10.1111/gcb.12320 CrossRefGoogle Scholar
  11. 11.
    Littman R, Willis BL, Pfeffer C, Bourne DG (2009) 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.  https://doi.org/10.1111/j.1574-6941.2009.00666.x CrossRefGoogle Scholar
  12. 12.
    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.  https://doi.org/10.1016/j.jembe.2009.01.012 CrossRefGoogle Scholar
  13. 13.
    Rouzé H, Lecellier G, Saulnier D, Berteaux-Lecellier V (2016) Symbiodinium clades A and D differentially predispose Acropora cytherea to disease and Vibrio spp. colonization. Ecol Evol 6:560–572.  https://doi.org/10.1002/ece3.1895 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10.  https://doi.org/10.3354/meps243001 CrossRefGoogle Scholar
  15. 15.
    Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340.  https://doi.org/10.1146/annurev-micro-102215-095440 CrossRefGoogle Scholar
  16. 16.
    Cardini U, Bednarz VN, Naumann MS et al (2015) Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc B Biol Sci 282:20152257.  https://doi.org/10.1098/rspb.2015.2257 CrossRefGoogle Scholar
  17. 17.
    Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000.  https://doi.org/10.1126/science.1099128 CrossRefGoogle Scholar
  18. 18.
    Wegley L, Edwards R, Rodriguez-Brito B et al (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719.  https://doi.org/10.1111/j.1462-2920.2007.01383.x CrossRefGoogle Scholar
  19. 19.
    Lema KA, Willis BL, Bourne DG, Bourneb DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78:3136–3144.  https://doi.org/10.1128/AEM.07800-11 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ritchie KB (1997) Physiological comparison of bacterial communities from various species of scleractinian corals. Physiological comparisons of bacterial communities from various species of scleractinian corals. Proc 8th Int Coral Reef Symp 1:521–526Google Scholar
  21. 21.
    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 143–156Google Scholar
  22. 22.
    Bayer T, Neave MJ, Alsheikh-Hussain A 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.  https://doi.org/10.1128/AEM.00695-13 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina JB et al (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274.  https://doi.org/10.1038/ismej.2015.39 CrossRefGoogle Scholar
  24. 24.
    Bourne DG, Dennis PG, Uthicke S et al (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7:1452–1458.  https://doi.org/10.1038/ismej.2012.172 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Roder C, Bayer T, Aranda M et al (2015) Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol 24:3501–3511.  https://doi.org/10.1111/mec.13251 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078.  https://doi.org/10.1007/s002270100674 CrossRefGoogle Scholar
  27. 27.
    Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawaii. Mol Phylogenet Evol 56:492–497.  https://doi.org/10.1016/j.ympev.2010.03.040 CrossRefGoogle Scholar
  28. 28.
    LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG et al (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603.  https://doi.org/10.1007/s00338-004-0428-4 CrossRefGoogle Scholar
  29. 29.
    Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts-symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43.  https://doi.org/10.1016/j.ppees.2006.04.001 CrossRefGoogle Scholar
  30. 30.
    Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc B Biol Sci 279:4352–4361.  https://doi.org/10.1098/rspb.2012.1454 CrossRefGoogle Scholar
  31. 31.
    Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci U S A 105:9256–9261.  https://doi.org/10.1073/pnas.0801328105 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral “bleaching” event. Proc Biol Sci 276:4139–4148.  https://doi.org/10.1098/rspb.2009.1405 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Stat M, Pochon X, Franklin EC et al (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3:1317–1329.  https://doi.org/10.1002/ece3.556 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174.  https://doi.org/10.1111/j.1462-2920.2005.00793.x CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134.  https://doi.org/10.2307/1542872 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Pochon X, Forsman ZH, Spalding HL et al (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawaii. R Soc Open Sci 2:140351CrossRefPubMedCentralGoogle Scholar
  37. 37.
    Pommier T, Canbäck B, Riemann L et al (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16:867–880.  https://doi.org/10.1111/j.1365-294X.2006.03189.x CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Poelen JH, Simons JD, Mungall CJ (2014) Global biotic interactions: an open infrastructure to share and analyze species-interaction datasets. Ecol Inform 24:148–159.  https://doi.org/10.1016/j.ecoinf.2014.08.005 CrossRefGoogle Scholar
  39. 39.
    Moitinho-Silva L, Nielsen S, Amir A et al (2017) The sponge microbiome project. Gigascience 6:1–7.  https://doi.org/10.1093/gigascience/gix077 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Bascompte JP, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6:69–81.  https://doi.org/10.1046/j.1461-0248.2003.00403.x CrossRefGoogle Scholar
  41. 41.
    Soffer N, Zaneveld J, Vega Thurber R (2014) Phage-bacteria network analysis and its implication for the understanding of coral disease. Environ Microbiol 17:1203–1218.  https://doi.org/10.1111/1462-2920.12553 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    McCliment E, Nelson CE, Carlson C et al (2012) An all-taxon microbial inventory of the Moorea coral reef ecosystem. ISME J 6:309–319.  https://doi.org/10.1038/ismej.2011.108 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Bonthond G, Merselis DG, Dougan KE et al (2018) Inter-domain microbial diversity within the coral holobiont Siderastrea siderea from two depth habitats. PeerJ 6:e4323.  https://doi.org/10.7717/peerj.4323 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Leite DC, Salles JF, Calderon EN et al (2018) Specific plasmid patterns and high rates of bacterial co-occurrence within the coral holobiont. Ecol Evol 8:1818–1832.  https://doi.org/10.1002/ece3.3717 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Huggett MJ, Apprill A (2018) Coral Microbiome Database: Integration of sequences reveals high diversity and relatedness of coralassociated microbes. Environmental microbiology reports.  https://doi.org/10.1111/1758-2229.12686
  46. 46.
    Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596.  https://doi.org/10.1093/nar/gks1219 CrossRefGoogle Scholar
  47. 47.
    Yilmaz P, Parfrey LW, Yarza P et al (2014) The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:643–648.  https://doi.org/10.1093/nar/gkt1209 CrossRefGoogle Scholar
  48. 48.
    Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Franklin EC, Stat M, Pochon X et al (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol Ecol Resour 12:369–373.  https://doi.org/10.1111/j.1755-0998.2011.03081.x CrossRefGoogle Scholar
  50. 50.
    Dubois P (2000) MySQL. New Riders Publishing, Indianapolis, INGoogle Scholar
  51. 51.
    Chanson H (2009) Applied hydrodynamics: an introduction to ideal and real fluid flows. CRC Press, Taylor & Francis Group, LeidenCrossRefGoogle Scholar
  52. 52.
    Thunell RC (1989) Red Sea salinity. Nature 339:21.  https://doi.org/10.1038/339021a0 CrossRefGoogle Scholar
  53. 53.
    LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: in search of a “species” level marker. J Phycol 37:866–880CrossRefGoogle Scholar
  54. 54.
    Sampayo EM, Dove S, Lajeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519.  https://doi.org/10.1111/j.1365-294X.2008.04037.x CrossRefGoogle Scholar
  55. 55.
    Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks:2498–2504.  https://doi.org/10.1101/gr.1239303 CrossRefPubMedCentralGoogle Scholar
  56. 56.
    Assenov Y et al (2008) Computing topological parameters of biological networks. Bioinformatics 24:282–284CrossRefGoogle Scholar
  57. 57.
    Kellogg C, Piceno YM, Tom LM et al (2013) Comparing bacterial community composition between healthy and white plague-like disease states in Orbicella annularis using PhyloChip™ G3 microarrays. PLoS One 8:e79801.  https://doi.org/10.1371/journal.pone.0079801 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Röthig T, Costa RM, Simona F et al (2016) Distinct bacterial communities associated with the coral model Aiptasia in aposymbiotic and symbiotic states with Symbiodinium. Front Mar Sci 3:234.  https://doi.org/10.3389/fmars.2016.00234 CrossRefGoogle Scholar
  59. 59.
    Raina JB, Clode PL, Cheong S et al (2017) Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. Elife 6:1–17.  https://doi.org/10.7554/eLife.23008 CrossRefGoogle Scholar
  60. 60.
    Stat M, Loh WKW, LaJeunesse TC et al (2009) Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713.  https://doi.org/10.1007/s00338-009-0509-5 CrossRefGoogle Scholar
  61. 61.
    McKew B, Dumbrell J, Daud SD et al (2012) Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 78:5229–5237.  https://doi.org/10.1128/AEM.07764-11 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367.  https://doi.org/10.1111/evo.12270 CrossRefGoogle Scholar
  63. 63.
    Hadaidi G, Röthig T, Yum LK et al (2017) Stable mucus-associated microbial communities in bleached and healthy corals of Porites lobata from Arabian Seas. Sci Rep 7:45326  https://doi.org/10.1038/srep45362 CrossRefGoogle Scholar
  64. 64.
    Lesser MP, Falcón LI, Rodríguez-Román A et al (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152.  https://doi.org/10.3354/meps07008 CrossRefGoogle Scholar
  65. 65.
    Radjasa OK, Salasia SIO, Sabdono A et al (2007) Antibacterial activity of marine bacterium Pseudomonas sp. associated with soft coral Sinularia polydactyla against Streptococcus equi subsp. zooepidemicus. Int J Pharmacol 3:170–117.  https://doi.org/10.3923/ijp.2007.170.174 CrossRefGoogle Scholar
  66. 66.
    Howard EC, Sun S, Reisch CR et al (2011) Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Appl Environ Microbiol 77:524–553.  https://doi.org/10.1128/AEM.01457-10 CrossRefGoogle Scholar
  67. 67.
    Raina JB, Tapiolas DM, Forêt S et al (2013) DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502:677–680.  https://doi.org/10.1038/nature12677 CrossRefGoogle Scholar
  68. 68.
    Leite DC, Leão P, Garrido AG et al (2017) Broadcast spawning coral Mussismilia hispida can vertically transfer its associated bacterial core. Front Microbiol 8:1–12.  https://doi.org/10.3389/fmicb.2017.00176 CrossRefGoogle Scholar
  69. 69.
    LaJeunesse TC, Bhagooli R, Hidaka M et al (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161.  https://doi.org/10.3354/meps284147 CrossRefGoogle Scholar
  70. 70.
    Lien YT, Fukami H, Yamashita Y (2013) Symbiodinium clade C among zooxanthellate corals (Scleractinia) in the temperate zone of Japan. Fish Sci 79:579–591.  https://doi.org/10.1007/s12562-013-0623-8 CrossRefGoogle Scholar
  71. 71.
    Tonk L, Sampayo EM, Weeks S et al (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLoS One 8:e68533.  https://doi.org/10.1371/journal.pone.0068533 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Cardini U, Bednarz VN, van Hoytema N et al (2016) Budget of primary production and dinitrogen fixation in a highly seasonal Red Sea coral reef. Ecosystems 19:771–785.  https://doi.org/10.1007/s10021-016-9966-1 CrossRefGoogle Scholar
  73. 73.
    Benavides M, Houlbrèque F, Camps M et al (2016) Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata. J Exp Biol 219:2608–2612.  https://doi.org/10.1242/jeb.139451 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Bednarz VN, Grover R, Maguer J-F et al (2017) The assimilation of diazotroph-derived nitrogen by Scleractinian corals depends on their metabolic status. MBio 8:1–14.  https://doi.org/10.1128/mBio.02058-16 CrossRefGoogle Scholar
  75. 75.
    Steinke M, Brading P, Kerrison P et al (2011) Concentrations of dimethylsulfoniopropionate and dimethyl sulfide are strain-specific in symbiotic dinoflagellates (Symbiodinium sp., Dinophyceae). J Phycol 47:775–783.  https://doi.org/10.1111/j.1529-8817.2011.01011.x CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Jones G, King S (2015) Dimethylsulphoniopropionate (DMSP) as an indicator of bleaching tolerance in Scleractinian corals. J Mar Sci Eng 3:444–465.  https://doi.org/10.3390/jmse3020444 CrossRefGoogle Scholar
  77. 77.
    Raina JB, Dinsdale E, Willis BL, Bourne DG (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18:101–108.  https://doi.org/10.1016/j.tim.2009.12.002 CrossRefGoogle Scholar
  78. 78.
    Pogoreutz C, Rädecker N, Cárdenas A et al (2017) Nitrogen fixation aligns with nifH abundance and expression in two coral trophic functional groups. Front Microbiol 8:1–7.  https://doi.org/10.3389/fmicb.2017.01187 CrossRefGoogle Scholar
  79. 79.
    Veron JEN (2002) New species described in corals of the world. Aust Inst Mar Sci Monogr Ser 11:1–206Google Scholar
  80. 80.
    Romano SL, Cairns SD (2000) Molecular phylogenetic hypothesis for the evolution of scleractinian corals. Bull Mar Sci 67:1043Google Scholar
  81. 81.
    Grupstra CGB, Coma R, Ribes M et al (2017) Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 36:981–985.  https://doi.org/10.1007/s00338-017-1589-2 CrossRefGoogle Scholar
  82. 82.
    Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and Eastern Pacific. Proc 8th Int Corall Reef Symp 2:1301–1306Google Scholar
  83. 83.
    LaJeunesse TC, Loh WKW, van Woesik R et al (2003) Low symbiont diversity in southern Great Barrier Reef corals relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054.  https://doi.org/10.4319/lo.2003.48.5.2046 CrossRefGoogle Scholar
  84. 84.
    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.  https://doi.org/10.1093/molbev/msi042 CrossRefGoogle Scholar
  85. 85.
    Stat M, Gates RD (2011) Clade D Symbiodinium in Scleractinian corals: a “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Biol 2011:1–9.  https://doi.org/10.1155/2011/730715 CrossRefGoogle Scholar
  86. 86.
    Pindell JL, Cande SC, Pitman WC et al (1988) A plate-kinematic framework for models of Caribbean evolution. Tectonophysics 155:121–138.  https://doi.org/10.1016/0040-1951(88)90262-4 CrossRefGoogle Scholar
  87. 87.
    Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259.  https://doi.org/10.1128/AEM.00554-06 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Sharon G, Rosenberg E (2010) Healthy corals maintain Vibrio in the VBNC state. Environ Microbiol Rep 2:116–119.  https://doi.org/10.1111/j.1758-2229.2009.00113.x CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Richardson L (1996) Horizontal and vertical migration patterns of Phormidium corallyticum and Beggiatoa spp. associated with Black-Band disease of corals. Microb Ecol 32:323–335.  https://doi.org/10.1007/s00248-006-9107-z CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    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.  https://doi.org/10.1128/AEM.68.5.2214-2228.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Garren M, Raymundo L, Guest J et al (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoSOne 4:e7319.  https://doi.org/10.1371/journal.pone.000731994 CrossRefGoogle Scholar
  92. 92.
    Rosenberg E, Kushmaro A, Kramarsky-Winter E et al (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146.  https://doi.org/10.1038/ismej.2008.104 CrossRefGoogle Scholar
  93. 93.
    Rosenberg E, Ben Haim Y (2002) Microbial disease of corals and global warming. Environ Microbiol 4:318–326CrossRefGoogle Scholar
  94. 94.
    Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302.  https://doi.org/10.3354/meps266273 CrossRefGoogle Scholar
  95. 95.
    Park E, Hwang DS, Lee JS et al (2012) Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Mol Phylogenet Evol 62:329–345.  https://doi.org/10.1016/j.ympev.2011.10.008 CrossRefPubMedGoogle Scholar
  96. 96.
    Gajigan AP, Diaz L, Conaco C (2017) Resilience of the prokaryotic microbial community of Acropora digitifera to elevated temperature. Microbiol Open 72:e00478–e00411.  https://doi.org/10.1002/mbo3.478 CrossRefGoogle Scholar
  97. 97.
    Ziegler M, Seneca FO, Yum LK et al (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:1–8.  https://doi.org/10.1038/ncomms14213 CrossRefGoogle Scholar
  98. 98.
    Harvell CD, Mitchell CE, Ward JR et al (2002) Climate warming and disease risks for terrestrial and marine biota. Sci 296:2158CrossRefGoogle Scholar
  99. 99.
    Vezzulli L, Previati M, Pruzzo C et al (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environ Microbiol 12:2007–2019.  https://doi.org/10.1111/j.1462-2920.2010.02209.x CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Baker-Austin C, Trinanes J, Taylor NGH et al (2012) Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang 3:73–77.  https://doi.org/10.1038/nclimate1628 CrossRefGoogle Scholar
  101. 101.
    Burge C, Mark Eakin C, Friedman CS et al (2014) Climate change influences on marine infectious diseases: implications for management and society. Annu Rev Mar Sci 6:249–277.  https://doi.org/10.1146/annurev-marine-010213-135029 CrossRefGoogle Scholar
  102. 102.
    Neave MJ, Michell CT, Apprill A, Voolstra CR (2017) Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci Rep 7:40579.  https://doi.org/10.1038/srep40579 CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Hernandez-Agreda A, Leggat W, Bongaerts P, Ainsworth TD (2016) The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio 7:e00560–e00516.  https://doi.org/10.1128/mBio.00560-16 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449.  https://doi.org/10.1128/AEM.01162-12 CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Pantos O, Bongaerts P, Dennis PG et al (2015) Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9:1–12.  https://doi.org/10.1038/ismej.2015.3 CrossRefGoogle Scholar
  106. 106.
    Lawson A, Raina JB, Kahlke T et al (2017) Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium. Environ Microbiol Rep 10(1):7–11.  https://doi.org/10.1111/1758-2229.12599 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Marine Ecosystems Research, School of ScienceEdith Cowan UniversityJoondalupAustralia
  2. 2.Trace and Environmental DNA LaboratoryDepartment of Environment and Agriculture Curtin UniversityBentleyWestern Australia
  3. 3.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  4. 4.Centre for Ecosystem Management, School of ScienceEdith Cowan UniversityJoondalupAustralia
  5. 5.School of Environmental and Life Sciences, Faculty of ScienceThe University of NewcastleOurimbahAustralia

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