Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals
Gorgonian corals serve as key engineering species within Mediterranean rocky-shore communities that have recently suffered from repeated mortality events during warm temperature anomalies. Among the factors that may link thermal conditions with disease outbreaks, a number of bacterial pathogens have been implicated; they may take advantage of decreases in the defenses and/or overall health of the gorgonian hosts. Considering the beneficial role of the resident bacteria in tropical coral holobionts, a detailed characterization of the gorgonian-associated microbial populations is required to better understand the relationships among native microbiota, host fitness, and pathogen susceptibility. In this study, the bacterial communities associated with three sympatric gorgonian species, Eunicella singularis, Eunicella cavolini, and Corallium rubrum, were investigated to provide insight into the stability and the specificity of host–microbe interactions. Natural variations in bacterial communities were detected using terminal restriction fragment length polymorphism (T-RFLP) of the 16S ribosomal DNA. No major differences were identified between individual colonies sampled in winter or in summer within each gorgonian species. Although hierarchical cluster analysis of the T-RFLP profiles revealed that the three species harbor distinct communities, comparison of the T-RFLP peaks indicated the presence of common bacterial ribotypes. From phylogenetic analysis of 16S rDNA clone libraries, we identified a bacterial lineage related to the Hahellaceae family within the Oceanospirillales that is shared among E. singularis, E. cavolini, and C. rubrum and that dominates the communities of both species of Eunicella. However, distinct clades of Hahellaceae are harbored by various gorgonian species from Mediterranean and tropical waters, suggesting that these bacteria have formed host-specific symbiotic relationships with gorgonian octocorals. In addition, the relatedness of symbionts from host species belonging to the same taxon but occurring in geographically remote areas is consistent with codivergence between gorgonians and their associated bacteria.
KeywordsGorgonians Corals Bacteria Hahellaceae Host specificity Mediterranean Sea
The authors gratefully acknowledge Olivier Bianchimani, Christian Marschal, and Frederic Zuberer for their help with field sampling. We thank Simon Bonato, Jérôme Paperou, and Caroline Rocher for assistance with the T-RFLP experiments and clone library construction. We further thank Marie Roumagnac for assistance regarding sequence analysis and three anonymous reviewers for their help improving the manuscript. This research was supported by the Total Foundation for Marine Biodiversity.
- Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195Google Scholar
- Bayer FM (1981) Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proc Biol Soc Wash 94:902–947Google Scholar
- Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (Northwestern Mediterranean), summer 1999. Ecol Lett 3:284–293CrossRefGoogle Scholar
- Daly M, Brugler MR, Cartwright P, Collins AG, Dawson MN, Fautin DG, France SC, McFadden CS, Opresko DM, Rodriguez E, Romano SL, Stake JL (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182Google Scholar
- Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonne P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Perez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103CrossRefGoogle Scholar
- Kolde R (2012) pheatmap: Pretty Heatmaps. R package version 0.7.4. http://cran.r-project.org/package=pheatmap
- Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2012) vegan: Community Ecology Package. R package version 2.0-5. http://cran.r-project.org/package=vegan
- Sanchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987Google 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:e10898]Google Scholar
- Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5:e9554]Google Scholar
- Vighi M (1972) Etude sur la reproduction de Corallium rubrum (L.). Vie Milieu 23:21–32Google Scholar
- Weinberg S, Weinberg F (1979) Life-cycle of a gorgonian—Eunicella singularis (Esper, 1794). Contrib Zool 48:127–140Google Scholar