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

Coral Reefs

Volumn 34, Issue 4, 2015, Pages 1087-1098

  La Rivière, Marie ^a   Garrabou, Joaquim ^a,b   Bally, Marc ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Bacteria; Corals; Gorgonians; Hahellaceae; Host specificity; Mediterranean Sea

Indexed keywords

BACTERIUM; CLUSTER ANALYSIS; CORAL REEF; DIVERGENCE; FITNESS; HOST SPECIFICITY; MORTALITY; PHYLOGENETICS; POPULATION OUTBREAK; ROCKY SHORE; SYMBIONT;

MEDITERRANEAN SEA;

ANTHOZOA; BACTERIA (MICROORGANISMS); CORALLIUM RUBRUM; EUNICELLA; EUNICELLA CAVOLINI; EUNICELLA SINGULARIS; GORGONACEA; GORGONIA; HAHELLACEAE; OCEANOSPIRILLALES;

EID: 84947129903     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-015-1334-7     Document Type: Article

References (64)

1. Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240
2. 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
3. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55:539–552
4. 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
5. Apprill A, Marlow HQ, Martindale MQ, Rappé MS (2009) The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3:685–699
6. 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
7. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195
8. 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
9. 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
10. 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
11. 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
12. Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. Kolde R (2012) pheatmap: Pretty Heatmaps. R package version 0.7.4. http://cran.r-project.org/package=pheatmap
30. 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
31. 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
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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
38. 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
39. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190
40. 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
41. 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
42. 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
43. 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
44. 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
45. 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
46. Roeselers G, Newton ILG (2012) On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl Microbiol Biotechnol 94:1–10
47. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
48. 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
49. Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39
50. Sanchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987
51. 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
52. 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]
53. 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
54. Southern EM (1979) Measurement of DNA length by gel electrophoresis. Anal Biochem 100:319–323
55. Speck MD, Donachie SP (2012) Widespread Oceanospirillaceae bacteria in Porites spp. J Mar Biol. doi:10.1155/2012/746720
56. 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
57. Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5:e9554]
58. 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
59. 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
60. 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
61. Vighi M (1972) Etude sur la reproduction de Corallium rubrum (L.). Vie Milieu 23:21–32
62. Webster NS, Bourne DG (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94
63. Weinberg S, Weinberg F (1979) Life-cycle of a gorgonian—Eunicella singularis (Esper, 1794). Contrib Zool 48:127–140
64. 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