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Mucus composition and bacterial communities associated with the tissue and skeleton of three scleractinian corals maintained under culture conditions

Published online by Cambridge University Press:  01 September 2010

Pascale Tremblay ,
Markus G. Weinbauer ,
Cécile Rottier ,
Yann Guérardel ,
Christian Nozais  and
Christine Ferrier-Pagès
Pascale Tremblay*
Affiliation:
Centre Scientifique de Monaco, Avenue St-Martin, MC-98000Monaco Departement de Biologie, Chimie et Géographie, Université du Québec à Rimouski, 300 allée des Ursulines, Rimouski, QC Canada G5L 3A1
Markus G. Weinbauer
Affiliation:
CNRS, Laboratoire d'Océanographie de Villefranche, Université Pierre et Marie Curie-Paris 6, 06230 Villefranche-sur-Mer, France
Cécile Rottier
Affiliation:
Centre Scientifique de Monaco, Avenue St-Martin, MC-98000Monaco
Yann Guérardel
Affiliation:
Unité de Glycobiologie Structurale et Fonctionnelle, CNRS, Institut Fédératif de Recherche 147, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq Cedex, France
Christian Nozais
Affiliation:
Departement de Biologie, Chimie et Géographie, Université du Québec à Rimouski, 300 allée des Ursulines, Rimouski, QC Canada G5L 3A1
Christine Ferrier-Pagès
Affiliation:
Centre Scientifique de Monaco, Avenue St-Martin, MC-98000Monaco
*
Correspondence should be addressed to: P. Tremblay, Centre Scientifique de Monaco, Avenue St-Martin, MC-98000Monaco email: [email protected]
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Abstract

Corals live in close association with bacterial communities, but the nature of the relationship is still poorly understood. In this study, three scleractinian coral species, Galaxea fascicularis, Pavona cactus and Turbinaria reniformis were incubated under different laboratory conditions, and the composition of the bacterial community associated with their tissue or skeleton was compared between species or between species and seawater using denaturing gradient gel electrophoresis (DGGE). The amount of dissolved organic carbon (DOC) excreted and the mucus glycoconjugate composition were also determined for each species. The aim of the study was to assess if the bacterial community composition was species-specific or linked either to the seawater composition, or to the quality and quantity of carbon released by each coral. Results obtained showed that DOC release was significantly different (P < 0.0001) for the three species, with the highest excretion rate for G. fascicularis. Also, the mucus of G. fascicularis and P. cactus mainly contained galactose and glucose whereas the mucus of T. reniformis contained more glucose and xylose. Cluster analyses of microbial community composition showed that the bacterial community was species-specific in the coral tissue but not in the skeleton, in all conditions. It remained specific when corals were incubated in the same or in different aquaria, and under different seawater renewal rates. Since DOC release rates and bacterial composition were both different according to the coral species considered, a link might be suggested between the two parameters. Sequencing of DGGE bands indicated that some bacterial phylotypes were consistently retrieved in all samples of a given species.

Keywords

coralsbacterial community compositionmucus16S rDNA
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 3 , May 2011 , pp. 649 - 657
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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References

REFERENCES

Ainsworth, T.D. and Hoegh-Guldberg, O. (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquatic Biology 4, 289–296.Google Scholar
Bourne, D.G. (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24, 304–312.CrossRefGoogle Scholar
Bourne, D.G. and Munn, C.B. (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environmental Microbiology 7, 1162–1174.CrossRefGoogle ScholarPubMed
Brown, B.E. and Bythell, J.C. (2005) Perspectives on mucus secretion in reefs corals. Marine Ecology Progress Series 296, 291–309.Google Scholar
Crossland, C.J. (1987) In situ release of mucus and DOC-lipid from the corals Acopora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6, 35–42.Google Scholar
Crossland, C.J., Barnes, D.J. and Borowitzka, M.A. (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Marine Biology 60, 81–90.CrossRefGoogle Scholar
Curtis, T.P., Sloan, W.T. and Scannell, J.W. (2002) Estimating prokaryotic diversity and its limits. Proceedings of the National Academy of Sciences of the United States of America 99, 10494–10499.CrossRefGoogle ScholarPubMed
DiSalvo, L.H. (1971) Regenerative functions and microbial ecology of coral reefs: labelled bacteria in a coral reef microcosm. Journal of Experimental Marine Biology and Ecology 7, 123–136.CrossRefGoogle Scholar
Ducklow, H.W. and Mitchell, R. (1979) Composition of mucus released by coral reef coelenterates. Limnology and Oceanography 24, 706–714.CrossRefGoogle Scholar
Ferguson, R.L., Buckley, E.N. and Palumbo, A.V. (1984) Response of marine bacterioplankton to differential filtration and confinement. Applied and Environmental Microbiology 47, 49–55.CrossRefGoogle ScholarPubMed
Ferrier-Pagès, C., Leclercq, N., Jaubert, J. and Pelegri, S.P. (2000) Enhancement of pico- and nanoplankton growth by coral exudates. Aquatic Microbial Ecology 21, 203–209.Google Scholar
Frias-Lopez, J., Zerkle, A.L., Bonheyo, G.T. and Fouke, B.W. (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Applied and Environmental Microbiology 68, 2214–2228.Google Scholar
Fromin, N., Hamelin, J., Tarnawski, S., Roesti, D., Jourdain-Miserez, K., Forestier, N., Teyssier-Cuvelle, S., Gillet, F., Aragno, M. and Rossi, P. (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environmental Microbiology 4, 634–643.Google Scholar
Garren, M., Smriga, S. and Azam, F. (2008) Gradients of coastal fish farm effluents and their effect on coral reef microbes. Environmental Microbiology 10, 2299–2312.CrossRefGoogle ScholarPubMed
Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W. and Vasta, G.R. (1999) Emerging marine diseases–climate links and anthropogenic factors. Science 285, 1505–1510.CrossRefGoogle ScholarPubMed
Herndl, G.J. and Velimiroz, B. (1986) Microheterotrophic utilization of mucus released by the Mediterranean coral Cladocora cespitosa. Marine Biology 90, 363–369.CrossRefGoogle Scholar
Hong, M.J., Yu, Y.T., Chen, C.A., Chiang, P.W. and Tang, S.L. (2009) Influence of species specificity and other factors on bacteria associated with the coral Stylophora pistillata in Taiwan. Applied and Environmental Microbiology 75, 7797–7806.CrossRefGoogle ScholarPubMed
Jones, R.J., Bowyer, J., Hoegh-Guldberg, O. and Blackall, L.L. (2004) Dynamics of temperature-related coral disease outbreak. Marine Ecology Progress Series 281, 63–77.Google Scholar
Klaus, J.S., Janse, I., Heikoop, J.M., Sanford, R.A. and Fouke, B.W. (2007) Coral microbial communities, zooxanthellae and mucus along gradient of seawater depth and coastal pollution. Environmental Microbiology 9, 1291–1305.CrossRefGoogle ScholarPubMed
Kooperman, N., Ben-Dove, E., Kramarsky-Winter, E., Barak, Z. and Kushmaro, A. (2007) Coral mucus-associated bacterial communities from natural and aquarium environments. FEMS Microbiology Letters 276, 106–113.Google Scholar
Lane, D.J. (1991) 16S/23S rRNA sequencing. In Stackebrandt, E. and Goodfellow, M. (eds) Nucleic acid techniques in bacterial systematics. Chichester: John Wiley & Sons, pp. 115–175.Google Scholar
Littman, R.A., Willis, B.L., Pfeffer, C. and Bourne, D.G. (2009) Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiology Ecology 68, 152–163.Google Scholar
McCloskey, L.R. and Muscatine, L. (1984) Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proceedings of the Royal Society of London B 222, 215–230.Google Scholar
Meikle, P., Richards, G.N. and Yellowlees, D. (1988) Structural investigations on the mucus from six species of coral. Marine Biology 99, 187–193.CrossRefGoogle Scholar
Muscatine, L., Falkowski, P.G., Porter, J.W. and Dubinsky, Z. (1984) Fate of photosynthetic fixed carbon in light -and shade- adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London B 222, 181–202.Google Scholar
Pantos, O., Cooney, R.P., Tissier, M.D.A.L., Barer, M.B., O'Donnell, A.G. and Bythell, J.C. (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environmental Microbiology 5, 370–382.Google Scholar
Penn, K., Wu, D., Eisen, J.A. and Ward, N. (2006) Characterization of bacterial communities associated with deep-sea corals on Gulf of Alaska seamounts. Applied and Environmental Microbiology 72, 1680–1683.CrossRefGoogle ScholarPubMed
Porter, J.W., Muscatine, L., Dubinsky, Z. and Falkowski, P.G. (1984) Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London B 222, 161–180.Google Scholar
Ritchie, K.B. (2006) Regulation of microbial population by coral surface mucus and mucus-associated bacteria. Marine Ecology Progress Series 322, 1–14.Google Scholar
Ritchie, K.B. and Smith, G.W. (1997) Physiological comparison of bacterial communities from various species of scleractinian corals. In Lessios, H.A. and Macintyre, I.G. (eds) Proceedings of the 8th International Coral Reef Symoposium, Panama City, Panama, 24–29 June 1996. Balboa: Smithsonian Tropical Research Institute, pp. 521–526.Google Scholar
Ritchie, K.B. and Smith, G.W. (2004) Microbial communities of coral surface mucopolysaccharide layers. In Rosenberg, E. and Loya, Y. (eds) Coral health and disease. Berlin: Springer-Verlag, pp. 259–264.CrossRefGoogle Scholar
Rohwer, F., Breitbart, M., Jara, J., Azam, F. and Knowlton, N. (2001) Diversity of bacteria associated with the Caribbean coral, Montastreae franksi. Coral Reefs 20, 85–91.Google Scholar
Rohwer, F., Seguritan, V., Azam, F. and Knowlton, N. (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243, 1–10.Google Scholar
Schäfer, H. and Muyzer, G. (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. In Paul, J.H. (ed.) Marine microbiology: methods in microbiology. San Diego, CA: Academic Press, pp. 425–468.CrossRefGoogle Scholar
Shashar, N., Cohen, Y., Loya, Y. and Sar, N. (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral–bacteria interactions. Marine Ecology Progress Series 111, 259–264.CrossRefGoogle Scholar
Smith, P.K., Khrohn, R.I., Hermanson, G.T., Malia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. and Klenk, D.C. (1985) Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 76–85.Google Scholar
Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R., Arrieta, J.M. and Herndl, G.J. (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proceedings of the National Academy of Sciences of the United States of America 103, 12115–12120.CrossRefGoogle ScholarPubMed
Sorokin, Y.I. (1973) Trophical role of bacteria in the ecosystem of the coral reef. Nature 242, 415–417.Google Scholar
Stackebrandt, E. and Ebers, J. (2006) Taxonomic parameters revisited: tarnished gold standard. Microbiology Today November 2006, 152–155.Google Scholar
Stimson, J. and Kinzie, R.A. (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen enrichment and control conditions. Journal of Experimental Marine Biology and Ecology 153, 63–74.CrossRefGoogle Scholar
Wild, C., Rasheed, M., Werner, U., Franke, U., Johnstone, R. and Huettel, M. (2004) Degradation and mineralization of coral mucus in reef environments. Marine Ecology Progress Series 267, 159–171.CrossRefGoogle Scholar
Wild, C., Woyt, H. and Huettel, M. (2005) Influence of coral mucus on nutrient fluxes in carbonates sands. Marine Ecology Progress Series 287, 87–98.CrossRefGoogle Scholar
Williams, W.N., Viner, A.B. and Broughton, W.L. (1987) Nitrogen fixation (acetylene reduction) associated with the living coral Acropora varialis. Marine Biology 94, 531–535.CrossRefGoogle Scholar
Winter, C., Moeseneder, M.M. and Herndl, G.J. (2001) Impact of UV radiation on bacterioplankton community composition. Applied and Environmental Microbiology 67, 665–672.Google Scholar
Zanetta, J.P., Timmerman, P. and Leroy, Y. (1999) Gas–liquid chromatography of the heptafluorobutyrate derivatives of the O-methyl-glycosides on capillary columns: a method for the quantitative determination of the monosaccharide composition of glycoproteins and glycolipids. Glycobiology 9, 255–266.Google Scholar