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Regulation of Bacterial Communities Through Antimicrobial Activity by the Coral Holobiont

  • Host Microbe Interactions
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Abstract

Interactions between corals and associated bacteria and amongst these bacterial groups are likely to play a key role in coral health. However, the complexity of these interactions is poorly understood. We investigated the functional role of specific coral-associated bacteria in maintaining microbial communities on the coral Acropora millepora (Ehrenberg 1834) and the ability of coral mucus to support or inhibit bacterial growth. Culture-independent techniques were used to assess bacterial community structures whilst bacterial culture was employed to assess intra- and inter-specific antimicrobial activities of bacteria. Members of Pseudoalteromonas and ribotypes closely related to Vibrio coralliilyticus displayed potent antimicrobial activity against a range of other cultured isolates and grew readily on detached coral mucus. Although such bacterial ribotypes would be expected to have a competitive advantage, they were rare or absent on intact and healthy coral colonies growing in situ (analysed using denaturing gradient gel electrophoresis and 16S rRNA gene sequencing). The most abundant bacterial ribotypes found on healthy corals were Gammaproteobacteria, previously defined as type A coral associates. Our results indicate that this group of bacteria and specific members of the Alphaproteobacteria described here as ‘type B associates’ may be important functional groups for coral health. We suggest that bacterial communities on coral are kept in check by a combination of host-derived and microbial interactions and that the type A associates in particular may play a key role in maintaining stability of microbial communities on healthy coral colonies.

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References

  1. Ainsworth T, Fine M, Roff G, Hoegh-Guldberg O (2008) Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. Isme Journal 2:67–73

    Article  PubMed  CAS  Google Scholar 

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  3. Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55

    Article  Google Scholar 

  4. Blazejak A, Kuever J, Erseus C, Amann R, Dubilier N (2006) Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase, and adenosine 5′-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl Environ Microbiol 72:5527–5536

    Article  PubMed  CAS  Google Scholar 

  5. Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. Isme Journal 2:350–363

    Article  PubMed  CAS  Google Scholar 

  6. Bruno JF, Selig ER (2007) Regional Decline of Coral Cover in the Indo-Pacific: Timing, Extent, and Subregional Comparisons. PLoS ONE 2(8): e711

    Article  PubMed  Google Scholar 

  7. Cervino J, Thompson FL, Gomez-Gil B, Lorence EA, Goreau TJ, Hayes RL, Winiarski-Cervino K, Smith GW, Hughen KA, Bartels E (2008) The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J Appl Microbiol 105:1658–1671

    Article  PubMed  CAS  Google Scholar 

  8. 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 31:312–319

    Article  PubMed  CAS  Google Scholar 

  9. Dubilier N, Amann R, Erseus C, Muyzer G, Park SY, Giere O, Cavanaugh CM (1999) Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochete Olavius loisae (Annelida). Mar Ecol Prog Ser 178:271–280

    Article  Google Scholar 

  10. Geffen Y, Rosenberg E (2005) Stress-induced rapid release of antibacterials by scleractinian corals. Mar Biol 146:931–935

    Article  Google Scholar 

  11. Gochfeld D, Aeby G (2008) Antibacterial chemical defenses in Hawaiian corals: possible protection from disease. Mar Ecol Prog Ser 362:119–128

    Article  Google Scholar 

  12. Harborne AR, Mumby PJ, Zychaluk K, Hedley JD, Blackwell PG (2006) Modeling the beta diversity of coral reefs. Ecology 87:2871–2881

    Article  PubMed  Google Scholar 

  13. Hill JE, Baiano JCF, Barnes AC (2009) Isolation of a novel strain of Bacillus pumilus from penaeid shrimp that is inhibitory against marine pathogens. Journal of Fish Diseases 32:1007–1016

    Article  PubMed  CAS  Google Scholar 

  14. Kelman D, Kashman Y, Rosenberg E, Kushmaro A, Loya Y (2006) Antimicrobial activity of red sea corals. Mar Biol 149:357–363

    Article  CAS  Google Scholar 

  15. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62

    Article  PubMed  Google Scholar 

  16. Koh EGL (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398

    Article  CAS  Google Scholar 

  17. Kooperman N, Ben-Dov E, Kramarsky-Winter E, Barak Z, Kushmaro A (2007) Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiol Lett 276:106–113

    Article  PubMed  CAS  Google Scholar 

  18. Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396–396

    Article  CAS  Google Scholar 

  19. Kvennefors ECE, Leggat W, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, Barnes AC (2010) Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Developmental and Comparative Immunology 34 (11): 1219–1229

    Article  PubMed  CAS  Google Scholar 

  20. Kvennefors ECE, 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 32:1582–1592

    Article  PubMed  CAS  Google Scholar 

  21. Kvennefors ECE, Roff G (2009) Evidence of cyanobacteria-like endosymbionts in Acroporid corals from the Great Barrier Reef. Coral Reefs 28:547–547

    Article  Google Scholar 

  22. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS ONE 5:e10401

    Article  PubMed  Google Scholar 

  23. Lane DJ (1991) 16S/23S rRNA sequencing. Wiley, New York

    Google Scholar 

  24. Lee OO, Qian PY (2004) Potential control of bacterial epibiosis on the surface of the sponge Mycale adhaerens. Aquat Microb Ecol 34:11–21

    Article  Google Scholar 

  25. Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Buchner YA, Lai T, Steppi S, Jobb G, Forester W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Koenig A, Liss T, Luemann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  28. Luna GM, Biavasco F, Danovaro R (2007) Bacteria associated with the rapid tissue necrosis of stony corals. Environ Microbiol 9:1851–1857

    Article  PubMed  CAS  Google Scholar 

  29. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  30. Nicolaisen MH, Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Methods 50:189–203

    Article  PubMed  CAS  Google Scholar 

  31. Nissimov JRE, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbial Letters 292:210–215

    Article  CAS  Google Scholar 

  32. Pantos O, Bythell JC (2006) Bacterial community structure associated with white band disease in the elkhorn coral Acropora palmata determined using culture-independent 16S rRNA techniques. Dis Aquat Org 69:79–88

    Article  PubMed  CAS  Google Scholar 

  33. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394

    Article  PubMed  CAS  Google Scholar 

  34. Rincon-Rosales R, Lloret L, Ponce E, Martinez-Romero E (2009) Rhizobia with different symbiotic efficiencies nodulate Acaciella angustissima in Mexico, including Sinorhizobium chiapanecum sp. nov. which has common symbiotic genes with Sinorhizobium mexicanum (vol 67, pg 103, 2009). FEMS Microbiol Ecol 68:255–255

    Article  PubMed  CAS  Google Scholar 

  35. Ritchie KB, Dennis JH, McGrath T, Smith GW (1994) Bacteria associated with bleached and nonbleached areas of Monastrea annularis. Proc Symp Nat Hist Bahamas 5:75–80

    Google Scholar 

  36. Ritchie KB, Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral Health and Disease. Springer, Berlin, pp 259–264

    Google Scholar 

  37. 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 

  38. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91

    Article  Google Scholar 

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

    Article  Google Scholar 

  40. Rohwer F, Kelley S (2004) Culture-independent analyses of coral associated microbes. In: Rosenberg E, Loya Y (eds) Coral Health and Disease. Springer, Berlin, pp 265–277

    Google Scholar 

  41. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology-Revue Canadienne De Zoologie 69:82–90

    Article  CAS  Google Scholar 

  42. Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488

    Article  PubMed  CAS  Google Scholar 

  43. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380

    Article  PubMed  CAS  Google Scholar 

  44. Sudheesh PS, Xu HS (2001) Pathogenicity of Vibrio parahaemolyticus in tiger prawn Penaeus monodon Fabricius: possible role of extracellular proteases. Aquaculture 196:37–46

    Article  CAS  Google Scholar 

  45. Sunagawa SDT, Piceno YM, Brodie EL, Desalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. Isme Journal 3:512–521

    Article  PubMed  CAS  Google Scholar 

  46. Sussman M, Willis B, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS ONE 3:e2393

    Article  PubMed  Google Scholar 

  47. Swofford LSD. PAUP*, phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer, Sunderland, 2000.

  48. Vandenberghe J, Thompson FL, Gomez-Gil B, Swings J (2003) Phenotypic diversity amongst Vibrio isolates from marine aquaculture systems. Aquaculture 219:9–20

    Article  Google Scholar 

  49. Vizcaino MI, Johnson WR, Kimes NE, Williams K, Torralba M, Nelson KE, Smith GW, Weil E, Moeller PD, Morris PJ (2009) Antimicrobial resistance of the coral pathogen Vibrio coralliilyticus and Caribbean sister phylotypes isolated from a diseased octocoral. Microb Ecol 59:646–657

    Article  Google Scholar 

  50. Ward JR, Lafferty KD (2004) The elusive baseline of marine disease: Are diseases in ocean ecosystems increasing? PLoS Biol 2:542–547

    CAS  Google Scholar 

  51. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This project was supported in part by grants from the PADI Foundation, the Australian Coral Reef Society and the Winifred Violet Scott Foundation.

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Correspondence to E. Charlotte E. Kvennefors.

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Kvennefors, E.C.E., Sampayo, E., Kerr, C. et al. Regulation of Bacterial Communities Through Antimicrobial Activity by the Coral Holobiont. Microb Ecol 63, 605–618 (2012). https://doi.org/10.1007/s00248-011-9946-0

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  • DOI: https://doi.org/10.1007/s00248-011-9946-0

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