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.
Similar content being viewed by others
References
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
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55
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
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
Bruno JF, Selig ER (2007) Regional Decline of Coral Cover in the Indo-Pacific: Timing, Extent, and Subregional Comparisons. PLoS ONE 2(8): e711
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
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
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
Geffen Y, Rosenberg E (2005) Stress-induced rapid release of antibacterials by scleractinian corals. Mar Biol 146:931–935
Gochfeld D, Aeby G (2008) Antibacterial chemical defenses in Hawaiian corals: possible protection from disease. Mar Ecol Prog Ser 362:119–128
Harborne AR, Mumby PJ, Zychaluk K, Hedley JD, Blackwell PG (2006) Modeling the beta diversity of coral reefs. Ecology 87:2871–2881
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
Kelman D, Kashman Y, Rosenberg E, Kushmaro A, Loya Y (2006) Antimicrobial activity of red sea corals. Mar Biol 149:357–363
Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62
Koh EGL (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398
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
Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396–396
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
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
Kvennefors ECE, Roff G (2009) Evidence of cyanobacteria-like endosymbionts in Acroporid corals from the Great Barrier Reef. Coral Reefs 28:547–547
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
Lane DJ (1991) 16S/23S rRNA sequencing. Wiley, New York
Lee OO, Qian PY (2004) Potential control of bacterial epibiosis on the surface of the sponge Mycale adhaerens. Aquat Microb Ecol 34:11–21
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
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
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
Luna GM, Biavasco F, Danovaro R (2007) Bacteria associated with the rapid tissue necrosis of stony corals. Environ Microbiol 9:1851–1857
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
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
Nissimov JRE, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbial Letters 292:210–215
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
Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394
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
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
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
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
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
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
Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488
Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380
Sudheesh PS, Xu HS (2001) Pathogenicity of Vibrio parahaemolyticus in tiger prawn Penaeus monodon Fabricius: possible role of extracellular proteases. Aquaculture 196:37–46
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
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
Swofford LSD. PAUP*, phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer, Sunderland, 2000.
Vandenberghe J, Thompson FL, Gomez-Gil B, Swings J (2003) Phenotypic diversity amongst Vibrio isolates from marine aquaculture systems. Aquaculture 219:9–20
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
Ward JR, Lafferty KD (2004) The elusive baseline of marine disease: Are diseases in ocean ecosystems increasing? PLoS Biol 2:542–547
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
Acknowledgements
This project was supported in part by grants from the PADI Foundation, the Australian Coral Reef Society and the Winifred Violet Scott Foundation.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(TXT 7 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-011-9946-0