Skip to main content
SpringerLink
Log in

Microbial Interactions on Coral Surfaces and Within the Coral Holobiont

  • Chapter
  • First Online:
The Cnidaria, Past, Present and Future

Abstract

Microbial communities associated with coral surfaces are diverse and complex. They play key roles in nutrient acquisition by coral holobionts and in responses to stressors and diseases. Members of coral-associated microbiota produce antimicrobial compounds, inhibit cell-to-cell signaling, and disrupt virulence in opportunistic pathogens. Characterization of coral-associated microbial communities suggests that metabolic capabilities define the core members of the communities. However, some taxonomic conservation is becoming evident in microbial communities associated with the same coral species and genera in different geographic regions. Even though shifts in the composition of coral microbiota often correlate with the appearance of signs of diseases and/or bleaching, it is not yet clear to what extent these shifts are a cause or a consequence of diseases. This chapter focuses on interactions within coral-associated microbial communities and suggests potentially interesting directions for future research.

Cory J. Krediet and Julie L. Meyer contributed equally to the preparation of this manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 379.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 379.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alagely A, Krediet CJ, Ritchie KB, Teplitski M (2011) Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J 5(10):1609–1620. doi:10.1038/ismej.2011.45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alavi M, Miller T, Erlandson K, Schneider R, Belas R (2001) Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ Microbiol 3(6):380–396

    Article  CAS  PubMed  Google Scholar 

  • Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann Rev Mar Sci 5(5):321–348. doi:10.1146/Annurev-Marine-121211-172241

    Article  PubMed  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008a) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446. doi:10.1073/pnas.0804478105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anthony SL, Page CA, Bourne DG, Willis BL (2008b) Newly characterized distinct phases of the coral disease ‘atramentous necrosis’ on the Great Barrier Reef. Dis Aquat Organ 81(3):255–259. doi:10.3354/dao01962

    Article  CAS  PubMed  Google Scholar 

  • Apprill A, Hughen K, Mincer T (2013) Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ Microbiol 15(7):2063–2072. doi:10.1111/1462-2920.12107

    Article  CAS  PubMed  Google Scholar 

  • Aronson RB, Bruno JF, Precht WF, Glynn PW, Harvell CD, Kaufman L, Rogers CS, Shinn EA, Valentine JF (2003) Causes of coral reef degradation. Science 302(5650):1502–1504

    Article  CAS  PubMed  Google Scholar 

  • Augustin R, Fraune S, Bosch TCG (2010) How Hydra senses and destroys microbes. Semin Immunol 22(1):54–58. doi:10.1016/J.Smim.2009.11.002

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Physiol 59:89–113. doi:10.1146/annurev.arplant.59.032607.092759

    CAS  Google Scholar 

  • Ban SS, Graham NA, Connolly SR (2014) Evidence for multiple stressor interactions and effects on coral reefs. Glob Chang Biol 20(3):681–697. doi:10.1111/gcb.12453

    Article  PubMed  Google Scholar 

  • Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, Li Y, Hambleton EA, Guse A, Oates ME, Gough J, Weis VM, Aranda M, Pringle JR, Voolstra CR (2015) The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci U S A 112(38):11893–11898. doi:10.1073/pnas.1513318112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK, Mincer T, Hughen K, Apprill A, Voolstra CR (2013) The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl Environ Microbiol 79(15):4759–4762. doi:10.1128/Aem.00695-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69(7):4236–4242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145(2):329–337. doi:10.1007/S00227-004-1309-7

    Article  CAS  Google Scholar 

  • Bieri T, Pringle JR (2016) Effects of algal and host genotypes on the bleaching of a symbiotic cnidarian in response to low pH. PLoS One (in review)

    Google Scholar 

  • Bieri T, Onishi M, Xiang T, Grossman AR, Pringle JR (2016) Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching. PLoS One 11(4):e0152693. doi:10.1371/journal.pone.0152693

    Google Scholar 

  • Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2(4):350–363. doi:10.1038/ismej.2007.112

    Article  CAS  PubMed  Google Scholar 

  • Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17(12):554–562. doi:10.1016/j.tim.2009.09.004

    Article  CAS  PubMed  Google Scholar 

  • Bourne DG, Dennis PG, Uthicke S, Soo RM, Tyson GW, Webster N (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7(7):1452–1458. doi:10.1038/ismej.2012.172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309. doi:10.3354/meps296291

    Article  CAS  Google Scholar 

  • Burge CA, Eakin CM, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, Petes LE, Prager KC, Weil E, Willis BL, Ford SE, Harvell CD (2014) Climate change influences on marine infectious diseases: implications for management and society. Ann Rev Mar Sci 6:249–277. doi:10.1146/Annurev-Marine-010213-135029

    Article  PubMed  Google Scholar 

  • Cardenas A, Rodriguez RL, Pizarro V, Cadavid LF, Arevalo-Ferro C (2012) Shifts in bacterial communities of two Caribbean reef-building coral species affected by white plague disease. ISME J 6(3):502–512. doi:10.1038/ismej.2011.123

    Article  CAS  PubMed  Google Scholar 

  • Chen MC, Cheng YM, Sung PJ, Kuo CE, Fang LS (2003) Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem Biophys Res Commun 308:586–595. doi:10.1016/S0006-291X(03)01428-1

    Article  CAS  PubMed  Google Scholar 

  • Chimetto LA, Brocchi M, Thompson CC, Martins RCR, Ramos HR, Thompson FL (2008) Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida. Syst Appl Microbiol 31(4):312–319. doi:10.1016/J.Syapm.2008.06.001

    Article  CAS  PubMed  Google Scholar 

  • Cline K, Wernerwashburne M, Andrews J, Keegstra K (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol 75(3):675–678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coddeville B, Maes E, Ferrier-Pages C, Guerardel Y (2011) Glycan profiling of gel forming mucus layer from the scleractinian symbiotic coral Oculina arbuscula. Biomacromolecules 12(6):2064–2073. doi:10.1021/bm101557v

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Suzuki S, Omori Y, Wong SK, Ijichi M, Kaneko R, Kameyama S, Tanimoto H, Hamasaki K (2015) Abundance and distribution of dimethylsulfoniopropionate degradation genes and the corresponding bacterial community structure at dimethyl sulfide hot spots in the tropical and subtropical pacific ocean. Appl Environ Microbiol 81(12):4184–4194. doi:10.1128/AEM.03873-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunning R, Silverstein RN, Silverstein RN, Baker AC (2015) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B 282(1809):20141725. doi:10.1098/rspb.2014.1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeBose JL, Lema SC, Nevitt GA (2008) Dimethylsulfoniopropionate as a foraging cue for reef fishes. Science 319(5868):1356–1356. doi:10.1126/Science.1151109

    Article  CAS  PubMed  Google Scholar 

  • Deschaseaux ESM, Jones GB, Deseo MA, Shepherd KM, Kiene RP, Swan HB, Harrison PL, Eyre BD (2014) Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol Oceanogr 59(3):758–768. doi:10.4319/Lo.2014.59.3.0758

    Article  CAS  Google Scholar 

  • Deutscher J (2008) The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11(2):87–93. doi:10.1016/j.mib.2008.02.007

    Article  CAS  PubMed  Google Scholar 

  • Dobretsov S, Teplitski M, Paul V (2009) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25(5):413–427. doi:10.1080/08927010902853516

    Article  CAS  PubMed  Google Scholar 

  • Dobretsov S, Teplitski M, Bayer M, Gunasekera S, Proksch P, Paul VJ (2011) Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 27(8):893–905. doi:10.1080/08927014.2011.609616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas AE (2003) Coral bleaching – how and why? Mar Pollut Bull 46(4):385–392. doi:10.1016/S0025-326X(03)00037-7

    Article  CAS  PubMed  Google Scholar 

  • Downs CA, Kramarsky-Winter E, Martinez J, Kushmaro A, Woodley CM, Loya Y, Ostrander GK (2009) Symbiophagy as a cellular mechanism for coral bleaching. Autophagy 5:211–216. doi:10.4161/auto.5.2.7405

    Article  CAS  PubMed  Google Scholar 

  • Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ Microbiol 11(1):268–276. doi:10.1111/j.1462-2920.2008.01774.x

    Article  PubMed  Google Scholar 

  • Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B 274(1629):3079–3085. doi:10.1098/rspb.2007.0711

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out? PLoS One 7:e39024. doi:10.1371/journal.pone.0039024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunne RP, Brown BE (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20:201–210. doi:10.1007/s003380100160

    Google Scholar 

  • Dykens J, Shick JM, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea-anemone Anthopleura elegantissima and its endosymbiotic algae. J Exp Biol 168:219–241

    CAS  Google Scholar 

  • Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20(9):2444–2449

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Liu M, Simister R, Webster NS, Thomas T (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J 7(5):991–1002. doi:10.1038/ismej.2012.165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18(10):455–463. doi:10.1016/J.Tim.2010.07.001

    Article  CAS  PubMed  Google Scholar 

  • Franklin D, Hoegh-Guldberg O, Jones R, Berges J (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130

    Article  Google Scholar 

  • Frydenborg BR, Krediet CJ, Teplitski M, Ritchie KB (2013) Temperature-dependent inhibition of opportunistic Vibrio pathogens by native coral commensal bacteria. Microb Ecol 67:392–401. doi:10.1007/s00248-013-0334-9

    Article  PubMed  Google Scholar 

  • Fusetani N, Toyoda T, Asai N, Matsunaga S, Maruyama T (1996) Montiporic acids A and B, cytotoxic and antimicrobial polyacetylene carboxylic acids from eggs of the scleractinian coral Montipora digitata. J Nat Prod 59(8):796–797

    Article  CAS  PubMed  Google Scholar 

  • Garren M, Azam F (2010) New method for counting bacteria associated with coral mucus. Appl Environ Microbiol 76(18):6128–6133. doi:10.1128/AEM.01100-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garren M, Son K, Raina JB, Rusconi R, Menolascina F, Shapiro OH, Tout J, Bourne DG, Seymour JR, Stocker R (2014) A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J 8(5):999–1007. doi:10.1038/Ismej.2013.210

    Article  CAS  PubMed  Google Scholar 

  • Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host-cell detachment in symbiotic cnidarians – implications for coral bleaching. Biol Bull 182:324–332. doi:10.2307/1542252

    Article  Google Scholar 

  • Gochfeld DJ, Aeby GS (2008) Antibacterial chemical defenses in Hawaiian corals provide possible protection from disease. Mar Ecol Prog Ser 362:119–128

    Article  Google Scholar 

  • Gochfeld DJ, Olson JB, Slattery M (2006) Colony versus population variation in susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea. Dis Aquat Organ 69(1):53–65

    Article  PubMed  Google Scholar 

  • Golberg K, Eltzov E, Shnit-Orland M, Marks RS, Kushmaro A (2011) Characterization of quorum sensing signals in coral-associated bacteria. Microb Ecol 61(4):783–792. doi:10.1007/s00248-011-9848-1

    Article  PubMed  Google Scholar 

  • Golberg K, Pavlov V, Marks RS, Kushmaro A (2013) Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling. Biofouling 29(6):669–682

    Article  CAS  PubMed  Google Scholar 

  • Goreau TF (1964) Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science 145:383–386. doi:10.1126/science.145.3630.383

    Article  CAS  PubMed  Google Scholar 

  • Gorke B, Stulke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6(8):613–624

    Article  PubMed  CAS  Google Scholar 

  • Grover R, Ferrier-Pages C, Maguer JF, Ezzat L, Fine M (2014) Nitrogen fixation in the mucus of Red Sea corals. J Exp Biol 217(22):3962–3963. doi:10.1242/Jeb.111591

    Article  PubMed  Google Scholar 

  • Haapkyla J, Unsworth RK, Flavell M, Bourne DG, Schaffelke B, Willis BL (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS One 6(2):e16893. doi:10.1371/journal.pone.0016893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanes SD, Kempf SC (2013) Host autophagic degradation and associated symbiont loss in response to heat stress in the symbiotic anemone, Aiptasia pallida. Invertebr Biol 132:95–107. doi:10.1111/ivb.12018

    Article  Google Scholar 

  • Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus AD, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases – climate links and anthropogenic factors. Science 285(5433):1505–1510

    Article  CAS  PubMed  Google Scholar 

  • Henke JM, Bassler BL (2004) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186(20):6902–6914. doi:10.1128/JB.186.20.6902-6914.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoegh-Guldberg O, Mccloskey LR, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red-Sea. Coral Reefs 5(4):201–204. doi:10.1007/Bf00300964

    Article  Google Scholar 

  • 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. doi:10.1126/Science.1152509

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Connell JH (1997) Multiple stressors on coral reefs: a long-term perspective. Symposium on the effects of multiple stressors on freshwater and marine ecosystems at the annual meeting of the American-Society-of-Limnology-and-Oceanography 44:932–940. doi:10.4319/lo.1999.44.3_part_2.0932

    Google Scholar 

  • Iguchi A, Shinzato C, Foret S, Miller DJ (2011) Identification of fast-evolving genes in the scleractinian coral Acropora using comparative EST analysis. PLoS One 6(6):e20140. doi:10.1371/journal.pone.0020140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaap WC (1979) Observations on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull Mar Sci 29:414–422

    Google Scholar 

  • Jatkar AA, Brown BE, Bythell JC, Guppy R, Morris NJ, Pearson JP (2010) Coral mucus: the properties of its constituent mucins. Biomacromolecules 11(4):883–888. doi:10.1021/bm9012106

    Article  CAS  PubMed  Google Scholar 

  • Jones RJ (2004) Testing the ‘photoinhibition’ model of coral bleaching using chemical inhibitors. Mar Ecol Prog Ser 284:133–145

    Article  CAS  Google Scholar 

  • Jones R (2005) The ecotoxicological effects of Photosystem II herbicides on corals. Mar Pollut Bull 51:495–506. doi:10.1016/j.marpolbul.2005.06.027

    Article  CAS  PubMed  Google Scholar 

  • Jones R, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99

    Article  CAS  Google Scholar 

  • Kim YM, Bouras N, Kay NNV, Strelkov SE (2010) Inhibition of photosynthesis and modification of the wheat leaf proteome by Ptr ToxB: a host-specific toxin from the fungal pathogen Pyrenophora tritici-repentis. Proteomics 10(16):2911–2926. doi:10.1002/Pmic.200900670

    Article  CAS  PubMed  Google Scholar 

  • Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH, Kiss H, Munk AC, Tapia R, Green L, Detter C, Bruce DC, Brettin TS, Colwell RR, Morris PJ (2011) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6:835–846. doi:10.1038/ismej.2011.154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kirst GO (1990) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 41:21–53. doi:10.1146/Annurev.Pp.41.060190.000321

    Article  CAS  Google Scholar 

  • 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. doi:10.1128/AEM.00554-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krediet CJ, Ritchie KB, Cohen M, Lipp EK, Sutherland KP, Teplitski M (2009a) Utilization of mucus from the coral Acropora palmata by the pathogen Serratia marcescens and by environmental and coral commensal bacteria. Appl Environ Microbiol 75(12):3851–3858. doi:10.1128/Aem.00457-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krediet CJ, Ritchie KB, Teplitski M (2009b) Catabolite regulation of enzymatic activities in a white pox pathogen and commensal bacteria during growth on mucus polymers from the coral Acropora palmata. Dis Aquat Organ 87(1–2):57–66. doi:10.3354/Dao02084

    Article  CAS  PubMed  Google Scholar 

  • Krediet CJ, Ritchie KB, Alagely A, Teplitski M (2013a) Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen. ISME J 7(5):980–990. doi:10.1038/ismej.2012.164

    Article  CAS  PubMed  Google Scholar 

  • Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013b) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc R Soc B 280(1755):20122328. doi:10.1098/Rspb.2012.2328

    Article  PubMed  PubMed Central  Google Scholar 

  • Krediet CJ, Denofrio JC, Caruso C, Burriesci MS, Cella K, Pringle JR (2015) Rapid, precise, and accurate counts of Symbiodinium cells using the Guava flow cytometer, and a comparison to other methods. PLoS One 10(8):e0135725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Microbiol 51(Pt 4):1383–1388

    Article  CAS  PubMed  Google Scholar 

  • Kuta KG, Richardson LL (2002) Ecological aspects of black band disease of corals: relationships between disease incidence and environmental factors. Coral Reefs 21(4):393–398. doi:10.1007/S00338-002-0261-6

    Google Scholar 

  • Kvennefors EC, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32(12):1582–1592. doi:10.1016/j.dci.2008.05.010

    Article  CAS  PubMed  Google Scholar 

  • Kvennefors EC, 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(3):605–618. doi:10.1007/s00248-011-9946-0

    Article  CAS  PubMed  Google Scholar 

  • Kvitt H, Rosenfeld H, Zandbank K, Tchernov D (2011) Regulation of apoptotic pathways by Stylophora pistillata (anthozoa, pocilloporidae) to survive thermal stress and bleaching. PLoS One 6:e28665. doi:10.1371/journal.pone.0028665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Tissier MDAA, Brown BE (1996) Dynamics of solar bleaching in the intertidal reef coral Goniastrea aspera at Ko Phuket, Thailand. Mar Ecol Prog Ser 136:235–244. doi:10.3354/meps136235

    Article  Google Scholar 

  • Lema KA, Willis BL, Bourne DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78(9):3136–3144. doi:10.1128/AEM.07800-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lema KA, Willis BL, Bourne DG (2014) Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ Microbiol 16(10):3345–3359

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16(3):187–192. doi:10.1007/S003380050073

    Article  Google Scholar 

  • Lesser MP (2007) Coral reef bleaching and global climate change: can corals survive the next century? Proc Natl Acad Sci U S A 104(13):5259–5260. doi:10.1073/pnas.0700910104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007a) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346(1–2):36–44. doi:10.1016/j.jembe.2007.02.015

    Article  Google Scholar 

  • Lesser MP, Falcon LI, Rodriguez-Roman A, Enriquez S, Hoegh-Guldberg O, Iglesias-Prieto R (2007b) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152. doi:10.3354/Meps07008

    Article  CAS  Google Scholar 

  • Littman RA, 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(2):152–163. doi:10.1111/j.1574-6941.2009.00666.x

    Article  CAS  PubMed  Google Scholar 

  • Looney EE, Sutherland KP, Lipp EK (2010) Effects of temperature, nutrients, organic matter and coral mucus on the survival of the coral pathogen, Serratia marcescens PDL100. Environ Microbiol 12(9):2479–2485. doi:10.1111/j.1462-2920.2010.02221.x

    Article  PubMed  Google Scholar 

  • Mao-Jones J, Ritchie KB, Jones LE, Ellner SP (2010) How microbial community composition regulates coral disease development. PLoS Biol 8(3):e1000345. doi:10.1371/journal.pbio.1000345

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB, Paul JH (2010) High frequency of horizontal gene transfer in the oceans. Science 330(6000):50. doi:10.1126/science.1192243

    Article  CAS  PubMed  Google Scholar 

  • McDaniel LD, Young EC, Ritchie KB, Paul JH (2012) Environmental factors influencing Gene Transfer Agent (GTA) mediated transduction in the subtropical ocean. PLoS One 7(8):e43506. doi:10.1371/journal.pone.0043506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McFall-Ngai M, Heath-Heckman EA, Gillette AA, Peyer SM, Harvie EA (2012) The secret languages of coevolved symbioses: insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 24(1):3–8. doi:10.1016/j.smim.2011.11.006

    Article  PubMed  Google Scholar 

  • McKew B, Dumbrell A, Daud S, Hepburn L, Thorpe E, Mogensen L, Whitby C (2012) Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 78(15):5229–5237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meikle P, Richards GN, Yellowlees D (1987) Structural determination of the oligosaccharide side-chains from a glycoprotein isolated from the mucus of the coral Acropora formosa. J Biol Chem 262(35):16941–16947

    CAS  PubMed  Google Scholar 

  • Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from 6 species of coral. Mar Biol 99(2):187–193. doi:10.1007/BF00391980

    Article  CAS  Google Scholar 

  • Meron D, Atias E, Kruh LI, Elifantz H, Minz D, Fine M, Banin E (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5(1):51–60. doi:10.1038/Ismej.2010.102

    Article  PubMed  Google Scholar 

  • Meyer JL, Paul VJ, Teplitski M (2014) Community shifts in the surface microbiomes of the coral Porites astreoides with unusual lesions. PLoS One 9(6):e100316. doi:10.1371/journal.pone.0100316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyer JL, Gunasekera SP, Scott RM, Paul VJ, Teplitski M (2015) Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria. ISME J 10:1204-1216. doi:10.1038/ismej.2015.184

    Google Scholar 

  • Molchanova VI, Ovodova RG, Ovodov YS, Elkin YN, Fernandez Santana V (1985) Studies of the polysaccharide moiety of corallan, a glycoprotein from Pseudopterogorgia americana. Carbohydr Res 141(2):289–293. doi:10.1016/S0008-6215(00)90460-9

    Article  CAS  Google Scholar 

  • 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(18):6438–6449. doi:10.1128/AEM.01162-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450(7166):98–101. doi:10.1038/nature06252

    Article  CAS  PubMed  Google Scholar 

  • Muscatine L, Mccloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26(4):601–611

    Article  CAS  Google Scholar 

  • Negri A, Vollhardt C, Humphrey C, Heyward A, Jones R, Eaglesham G, Fabricius K (2005) Effects of the herbicide diuron on the early life history stages of coral. Mar Pollut Bull 51:370–383. doi:10.1016/j.marpolbul.2004.10.053

    Article  CAS  PubMed  Google Scholar 

  • Negri AP, Flores F, Röthig T, Uthicke S (2011) Herbicides increase the vulnerability of corals to rising sea surface temperature. Limnol Oceanogr 56:471–485. doi:10.4319/lo.2011.56.2.0471

    Article  CAS  Google Scholar 

  • Nevitt GA (2011) The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical. Integr Comp Biol 51(5):819–825. doi:10.1093/Icb/Icr093

    Article  CAS  PubMed  Google Scholar 

  • Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. doi:10.1146/annurev-genet-102108-134304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL (2011) Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol 79(6):1407–1417. doi:10.1111/j.1365-2958.2011.07548.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292(2):210–215. doi:10.1111/j.1574-6968.2009.01490.x

    Article  CAS  PubMed  Google Scholar 

  • Olson JB, Thacker RW, Gochfeld DJ (2014) Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge Aplysina cauliformis. FEMS Microbiol Ecol 87(1):268–279. doi:10.1111/1574-6941.12222

    Article  CAS  PubMed  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333(6041):418–422. doi:10.1126/Science.1204794

    Article  CAS  PubMed  Google Scholar 

  • Pantos O, Bongaerts P, Dennis PG, Tyson GW, Hoegh-Guldberg O (2015) Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix. ISME J 9(9):1916–1927. doi:10.1038/ismej.2015.3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul JH, Deflaun MF, Jeffrey WH (1986) Elevated levels of microbial activity in the coral surface microlayer. Mar Ecol Prog Ser 33(1):29–40

    Article  Google Scholar 

  • Paxton CW, Davy SK, Weis VM (2013) Stress and death of cnidarian host cells play a role in cnidarian bleaching. J Exp Biol 216:2813–2820. doi:10.1242/jeb.087858

    Article  PubMed  Google Scholar 

  • Pernice M, Dunn SR, Miard T, Dufour S, Dove S, Hoegh-Guldberg O (2011) Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PLoS One 6(6):e16095. doi:10.1371/journal.pone.0016095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Post DM, Yu L, Krasity BC, Choudhury B, Mandel MJ, Brennan CA, Ruby EG, McFall-Ngai MJ, Gibson BW, Apicella MA (2012) O-antigen and core carbohydrate of Vibrio fischeri lipopolysaccharide: composition and analysis of their role in Euprymna scolopes light organ colonization. J Biol Chem 287(11):8515–8530. doi:10.1074/jbc.M111.324012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 8:490–497. doi:10.1016/j.tim.2015.03.008

    Article  CAS  Google Scholar 

  • Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75(11):3492–3501. doi:10.1128/AEM.02567-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reidling JC, Miller MA, Steele RE (2000) Sweet Tooth, a novel receptor protein-tyrosine kinase with C-type lectin-like extracellular domains. J Biol Chem 275(14):10323–10330

    Article  CAS  PubMed  Google Scholar 

  • Reitzel AM, Sullivan JC, Traylor-Knowles N, Finnerty JR (2008) Genomic survey of candidate stress-response genes in the estuarine anemone Nematostella vectensis. Biol Bull 214(3):233–254

    Article  PubMed  Google Scholar 

  • Reynaud S, Leclercq N, Romaine-Liuod S, Ferrier-Pages C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Chang Biol 9:1660–1668. doi:10.1046/j.1529-8817.2003.00678.x

    Article  Google Scholar 

  • Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198. doi:10.1111/j.1742-4658.2006.05414.x

    Article  CAS  PubMed  Google Scholar 

  • Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    Article  CAS  Google Scholar 

  • Ritchie KB (2011) Bacterial symbionts of corals and Symbiodinium. In: Rosenberg E, Gophna U (eds) Beneficial microorganisms in multicellular life forms. Springer, Berlin, pp 139–150

    Google Scholar 

  • Rodriguez-Lanetty M, Granados-Cifuentes C, Barberan A, Bellantuono AJ, Bastidas C (2013) Ecological inferences from a deep screening of the complex bacterial consortia associated with the coral, Porites astreoides. Mol Ecol 22(16):4349–4362. doi:10.1111/mec.12392

    Article  CAS  PubMed  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10. doi:10.3354/Meps243001

    Article  Google Scholar 

  • Rosenberg E, Falkovitz L (2004) The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu Rev Microbiol 58:143–159. doi:10.1146/annurev.micro.58.030603.123610

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg E, Zilber-Rosenberg I (2011) Symbiosis and development: the hologenome concept. Birth Defects Res C, EmbryoToday: Rev 93(1):56–66. doi:10.1002/bdrc.20196

    Article  CAS  Google Scholar 

  • 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(5):355–362. doi:10.1038/nrmicro1635

    Article  CAS  PubMed  Google Scholar 

  • Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12(1):28–39. doi:10.1111/j.1462-2920.2009.02027.x

    Article  CAS  PubMed  Google Scholar 

  • Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204(20):3443–3456

    CAS  PubMed  Google Scholar 

  • Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293. doi:10.4319/lo.2006.51.3.1284

    Article  CAS  Google Scholar 

  • Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56(5):481–488. doi:10.1007/s00284-008-9100-5

    Article  CAS  PubMed  Google Scholar 

  • 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(5):e10898. doi:10.1371/journal.pone.0010898

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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. doi:10.1038/ismej.2011.144

    Article  CAS  PubMed  Google Scholar 

  • Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476(7360):320–323. doi:10.1038/nature10249

    Article  CAS  PubMed  Google Scholar 

  • Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67(3):371–380. doi:10.1111/j.1574-6941.2008.00644.x

    Article  CAS  PubMed  Google Scholar 

  • Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Chang Biol 11:1–11. doi:10.1111/j.1365-2486.2004.00895.x

    Article  Google Scholar 

  • Speck MD, Donachie SP (2012) Widespread Oceanospirillaceae bacteria in Porites spp. J Mar Biol Suppl 746720:746721–746727

    Google Scholar 

  • Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertel W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48(6):1433–1447. doi:10.1111/J.1529-8817.2012.01231.X

    Article  PubMed  Google Scholar 

  • Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009a) Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3(5):512–521. doi:10.1038/Ismej.2008.131

    Article  CAS  PubMed  Google Scholar 

  • Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, Weis VM, Medina M, Schwarz JA (2009b) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10:258. doi:10.1186/1471-2164-10-258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS One 3(6):e2393. doi:10.1371/journal.pone.0002393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG (2009) Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS One 4(2):e4511. doi:10.1371/journal.pone.0004511

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tait K, Hutchison Z, Thompson FL, Munn CB (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep 2(1):145–150. doi:10.1111/J.1758-2229.2009.00122.X

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi:10.1016/j.tplants.2008.01.005

    Article  CAS  PubMed  Google Scholar 

  • Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, Falkowski PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci U S A 108:9905–9909. doi:10.1073/pnas.1106924108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teplitski M, Rajamani S (2011) Signal and nutrient exchange in the interactions between soil algae and bacteria. In: Witzany G (ed) Biocommunication in soil microorganisms. Springer, Berlin, pp 413–426

    Chapter  Google Scholar 

  • Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-Acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111(1):100–116. doi:10.1021/Cr100045m

    Article  CAS  PubMed  Google Scholar 

  • Tolleter D, Seneca FO, DeNofrio JC, Krediet CJ, Palumbi SR, Pringle JR, Grossman AR (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23(18):1782–1786

    Article  CAS  PubMed  Google Scholar 

  • 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(3):649–657. doi:10.1017/S002531541000130x

    Article  CAS  Google Scholar 

  • Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pages C (2012) Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215(Pt 8):1384–1393. doi:10.1242/jeb.065201

    Article  CAS  PubMed  Google Scholar 

  • Vacelet E, Thomassin B (1991) Microbial utilization of coral mucus in long term in situ incubation over a coral reef. Hydrobiologia 211(1):19–32. doi:10.1007/BF00008613

    Article  Google Scholar 

  • van Dam JW, Uthicke S, Beltran VH, Mueller JF, Negri aP (2015) Combined thermal and herbicide stress in functionally diverse coral symbionts. Environ Pollut 204:271–279. doi:10.1016/j.envpol.2015.05.013

    Article  PubMed  CAS  Google Scholar 

  • Vezzulli L, Pezzati E, Huete-Stauffer C, Pruzzo C, Cerrano C (2013) 16SrDNA Pyrosequencing of the Mediterranean Gorgonian Paramuricea clavata reveals a link among alterations in bacterial holobiont members, anthropogenic influence and disease outbreaks. PLoS One 8(6):e67745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidal-Dupiol J, Ladriere O, Meistertzheim AL, Foure L, Adjeroud M, Mitta G (2011) Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus. J Exp Biol 214(Pt 9):1533–1545. doi:10.1242/jeb.053165

    Article  CAS  PubMed  Google Scholar 

  • Vine NG, Leukes WD, Kaiser H (2004) In vitro growth characteristics of five candidate aquaculture probiotics and two fish pathogens grown in fish intestinal mucus. FEMS Microbiol Lett 231(1):145–152

    Article  CAS  PubMed  Google Scholar 

  • Voss JD, Richardson LL (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25(4):569–576. doi:10.1007/S00338-006-0131-8

    Article  Google Scholar 

  • Wall CB, Fan TY, Edmunds PJ (2014) Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum. Coral Reefs 33:119–130. doi:10.1007/s00338-013-1085-2

    Article  Google Scholar 

  • Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 6:1–19. doi:10.3389/Fpls.2015.00085

  • Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164. doi:10.1038/nclimate1661

    Article  CAS  Google Scholar 

  • Wooldridge SA (2009) Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751. doi:10.1016/j.marpolbul.2008.12.013

    Article  CAS  PubMed  Google Scholar 

  • Zimmer BL, May AL, Bhedi CD, Dearth SP, Prevatte CW, Pratte Z, Campagna SR, Richardson LL (2014) Quorum Sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLoS One 9(9):e108541. doi:10.1371/journal.pone.0108541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

Preparation of this manuscript was supported by the Protect Our Reefs Foundation (MT, KBR, CJK and JLM) and by the George E. Burch Fellowship in Theoretical Medicine (MT).

Author information

Authors and Affiliations

  1. Smithsonian Marine Station, 701 Seaway Dr., Ft. Pierce, FL, 34949, USA

    Max Teplitski

  2. Department of Marine Science, Eckerd College, 4200 54th Ave S, St. Petersburg, FL, 33711, USA

    Cory J. Krediet

  3. Soil and Water Science Department, University of Florida, 2033 Mowry Rd, Gainesville, FL, 32611, USA

    Julie L. Meyer

  4. Mote Marine Laboratory, 1600 Ken Thompson Pkwy, Sarasota, FL, 34236, USA

    Kim B. Ritchie

Authors
  1. Max Teplitski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cory J. Krediet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie L. Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kim B. Ritchie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Max Teplitski .

Editor information

Editors and Affiliations

  1. Biological, Geological and Env Scie, University of Bologna, Bologna, Italy

    Stefano Goffredo

  2. Fac. Life Sciences, Bar-Ilan University, Ramat-Gan, Israel

    Zvy Dubinsky

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Teplitski, M., Krediet, C.J., Meyer, J.L., Ritchie, K.B. (2016). Microbial Interactions on Coral Surfaces and Within the Coral Holobiont. In: Goffredo, S., Dubinsky, Z. (eds) The Cnidaria, Past, Present and Future. Springer, Cham. https://doi.org/10.1007/978-3-319-31305-4_21

Download citation

Publish with us

Policies and ethics

Search

Navigation