Skip to main content
SpringerLink
Log in

Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240

    Article  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  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 15:2063–2072

    Article  CAS  PubMed  Google Scholar 

  • Apprill A, Marlow HQ, Martindale MQ, Rappé MS (2009) The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3:685–699

    Article  PubMed  Google Scholar 

  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195

    Google Scholar 

  • Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Glob Chang Biol 13:2078–2088

    Article  Google Scholar 

  • Bayer FM (1981) Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proc Biol Soc Wash 94:902–947

    Google Scholar 

  • Bayer T, Arif C, Ferrier-Pages C, Zoccola D, Aranda M, Voolstra CR (2013a) Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar Ecol Prog Ser 479:75–84

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ceh J, van Keulen M, Bourne DG (2013) Intergenerational transfer of specific bacteria in corals and possible implications for offspring fitness. Microb Ecol 65:227–231

    Article  CAS  PubMed  Google 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 3:284–293

    Article  Google Scholar 

  • Coma R, Ribes M, Zabala M, Gili JM (1995) Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Mar Ecol Prog Ser 117:173–183

    Article  Google Scholar 

  • Crisci C, Bensoussan N, Romano JC, Garrabou J (2011) Temperature anomalies and mortality events in marine communities: insights on factors behind differential mortality impacts in the NW Mediterranean. PLoS One 6:e23814

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Croquer A, Bastidas C, Elliott A, Sweet M (2013) Bacterial assemblages shifts from healthy to yellow band disease states in the dominant reef coral Montastraea faveolata. Environ Microbiol Rep 5:90–96

    Article  PubMed  Google 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 1668:127–182

    Google Scholar 

  • de Castro AP, Araujo SD, Reis AMM, Moura RL, Francini-Filho RB, Pappas G, Rodrigues TB, Thompson FL, Krüger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from Eastern Brazil. Microb Ecol 59:658–667

    Article  PubMed  Google Scholar 

  • Erpenbeck D, Breeuwer JAJ, van der Velde HC, van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141:377–386

    Article  Google Scholar 

  • Frydenborg BR, Krediet CJ, Teplitski M, Ritchie KB (2014) Temperature-dependent inhibition of opportunistic Vibrio pathogens by native coral commensal bacteria. Microb Ecol 67:392–401

    Article  PubMed  Google 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 15:1090–1103

    Article  Google Scholar 

  • Garren M, Raymundo L, Guest J, Harvell CD, Azam F (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4:e7309

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hansson L, Agis M, Maier C, Weinbauer MG (2009) Community composition of bacteria associated with cold-water coral Madrepora oculata: within and between colony variability. Mar Ecol Prog Ser 397:89–102

    Article  CAS  Google Scholar 

  • Jessen C, Villa Lizcano JF, Bayer T, Roder C, Aranda M, Wild C, Voolstra CR (2013) In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS One 8:e62091

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klaus JS, Frias-Lopez J, Bonheyo GT, Heikoop JM, Fouke BW (2005) Bacterial communities inhabiting the healthy tissues of two Caribbean reef corals: interspecific and spatial variation. Coral Reefs 24:129–137

    Article  Google Scholar 

  • Kolde R (2012) pheatmap: Pretty Heatmaps. R package version 0.7.4. http://cran.r-project.org/package=pheatmap

  • Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc R Soc Lond B Biol Sci 280:20122328

    Article  Google Scholar 

  • Kvennefors EC, 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 Central  PubMed  Google Scholar 

  • La Rivière M, Roumagnac M, Garrabou J, Bally M (2013) Transient shifts in bacterial communities associated with the temperate gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea. PLoS One 8:e57385

    Article  PubMed Central  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lee OO, Yang J, Bougouffa S, Wang Y, Batang Z, Tian R, Al-Suwailem A, Qian PY (2012) Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing. Appl Environ Microbiol 78:7173–7184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, Bachleitner M, Schleifer KH (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568

    Article  CAS  PubMed  Google Scholar 

  • Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    PubMed Central  CAS  PubMed  Google Scholar 

  • Martin Y, Bonnefont JL, Chancerelle L (2002) Gorgonians mass mortality during the 1999 late summer in French Mediterranean coastal waters: the bacterial hypothesis. Water Res 36:779–782

    Article  CAS  PubMed  Google Scholar 

  • McFadden CS, France SC, Sánchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phylogenet Evol 41:513–527

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  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 78:6438–6449

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mouchka ME, Hewson I, Harvell CD (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50:662–674

    Article  PubMed  Google Scholar 

  • 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

  • Osborn AM, Moore ER, Timmis KN (2000) An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2:39–50

    Article  CAS  PubMed  Google Scholar 

  • Osborne CA, Rees GN, Bernstein Y, Janssen PH (2006) New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72:1270–1278

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75:2495–2505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roeselers G, Newton ILG (2012) On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl Microbiol Biotechnol 94:1–10

    Article  PubMed Central  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

    Article  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 5:355–362

    Article  CAS  PubMed  Google Scholar 

  • Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39

    Article  CAS  PubMed  Google Scholar 

  • Sanchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987

    Google Scholar 

  • Schöttner S, Wild C, Hoffmann F, Boetius A, Ramette A (2012) Spatial scales of bacterial diversity in cold-water coral reef ecosystems. PLoS One 7:e32093

    Article  PubMed Central  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:e10898]

  • 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 6:790–801

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Southern EM (1979) Measurement of DNA length by gel electrophoresis. Anal Biochem 100:319–323

    Article  CAS  PubMed  Google Scholar 

  • Speck MD, Donachie SP (2012) Widespread Oceanospirillaceae bacteria in Porites spp. J Mar Biol. doi:10.1155/2012/746720

    Google Scholar 

  • Stakebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  Google Scholar 

  • Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5:e9554]

  • Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130

    Article  PubMed  Google Scholar 

  • Vega Thurber RL, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163

    Article  PubMed  Google Scholar 

  • Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environ Microbiol 12:2007–2019

    Article  CAS  PubMed  Google Scholar 

  • Vighi M (1972) Etude sur la reproduction de Corallium rubrum (L.). Vie Milieu 23:21–32

    Google Scholar 

  • Webster NS, Bourne DG (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94

    Article  CAS  PubMed  Google Scholar 

  • Weinberg S, Weinberg F (1979) Life-cycle of a gorgonian—Eunicella singularis (Esper, 1794). Contrib Zool 48:127–140

    Google Scholar 

  • Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7:57

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, 13288, Marseille, France

    Marie La Rivière, Joaquim Garrabou & Marc Bally

  2. Institut de Ciències del Mar (ICM-CSIC), 08003, Barcelona, Spain

    Joaquim Garrabou

Authors
  1. Marie La Rivière
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joaquim Garrabou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marc Bally
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc Bally.

Additional information

Communicated by Biology Editor Dr. Ruth D. Gates

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

La Rivière, M., Garrabou, J. & Bally, M. Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals. Coral Reefs 34, 1087–1098 (2015). https://doi.org/10.1007/s00338-015-1334-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-015-1334-7

Keywords

Search

Navigation