Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae)

Environmental Microbiology

Volumn 10, Issue 2, 2008, Pages 433-445

  Duperron, Sébastien ^a,b   Halary, Sébastien ^a,c   Lorion, Julien ^a   Sibuet, Myriam ^b   Gaill, Françoise ^a  

^a Université Pierre et Marie Curie ^*  (France)

^b IFREMER   (France)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

ANIMAL; ARTICLE; BACTEROIDETES; CLASSIFICATION; COLD; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENETICS; GILL; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MEDITERRANEAN SEA; MICROBIOLOGY; MOLECULAR GENETICS; MYTILIDAE; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS;

ANIMALS; BACTEROIDETES; COLD; DNA, BACTERIAL; GAMMAPROTEOBACTERIA; GILLS; IN SITU HYBRIDIZATION, FLUORESCENCE; MEDITERRANEAN SEA; MOLECULAR SEQUENCE DATA; MYTILIDAE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BACTERIA (MICROORGANISMS); BATHYMODIOLUS HECKERAE; BIVALVIA; GORGONACEA; IDAS; MYTILIDAE;

EID: 38049156401     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01465.x     Document Type: Article

References (61)

1. Abramoff, M.D., Magelhaes, P.J. Ram, S.J. (2004) Image processing with ImageJ. Biophot Int 11 : 36 42.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. Mol Biol 215 : 403 410.
3. Baco, A.R. Smith, C.R. (2003) High species richness in deep-sea-chemoautotrophic whale skeleton communities. Mar Ecol Prog Ser 260 : 109 114.
4. Bandi, C., Damiani, G., Magrassi, L., Grigolo, A., Fani, R. Sacchi, L. (1994) Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B Biol Sci 257 : 43 48.
5. Bano, N. Hollibaugh, J.T. (2002) Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl Environ Microbiol 68 : 505 518.
6. Bayon, G., Loncke, L., Dupré, S., Caprais, J.C., Ducassou, E., Duperron, S. (2007) submittted.
7. 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 alphaproteobacterias symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl Environ Microbiol 72 : 5527 5536.
8. Bolotin, J., Hrs-Brenko, M., Tutman, P., Glavic, N., Kozul, V., Skaramuca, B., et al. (2005) First record of Idas simpsonii (Mollusca: Bivalvia: Mytilidae) in the Adriatic Sea. J Mar Biolog Assoc UK 85 : 977 978.
9. Brown, M.W., Schwalbach, M.S., Hewson, I. Fuhrman, J.A. (2005) Coupling 16S-ITS rDNA clone libraries and ARISA to show marine microbial diversity: development and application to a time series. Environ Microbiol 7 : 1466 1479.
10. Cavanaugh, C.M., Levering, P.R., Maki, J.S., Mitchell, R. Lidstrom, M.E. (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325 : 346 347.
11. 4 at the Mid-Atlantic Ridge hyderothermal vent fields. Cah Biol Mar 43 : 259 262.
12. Cole, J.R., Chai, B., Marsh, T.L., Farris, R.J., Wang, Q., Kulam, S.A., et al. (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31 : 442 443.
13. DeChaine, E.G. Cavanaugh, C.M. (2005) Symbioses of methanotrophs and deep-sea mussels (Mytilidae: Bathymodiolinae). In Molecular Basis of Symbiosis. Overmann, J. (ed.). Berlin, Germany : Springer-Verlag, pp. 227 249.
14. DeChaine, E.G., Bates, A.E., Shank, T. Cavanaugh, C.M. (2006) Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal fields. Environ Microbiol 8 : 1902 1912.
15. Delwiche, C.F. Palmer, J.D. (1996) Rampant horizontal transfer and duplication of RubisCO genes in eubacteria and plastids. Mol Biol Evol 13 : 873 882.
16. Deming, J.W., Reysenbach, A.L., Macko, S.A. Smith, C.R. (1997) Evidence for the microbial basis of a chemoautotrophic invertebrate community at a whale fall on the deep seafloor: bone-colonizing bacteria and invertebrate endosymbionts. Microsc Res Tech 37 : 162 170.
17. Deplancke, B., Hristova, K.R., Oakley, H.A., McCracken, V.J., Aminov, R., Mackie, R.I. Gaskins, H.R. (2000) Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl Environ Microbiol 66 : 2166 2174.
18. Distel, D.L. Cavanaugh, C.M. (1994) Independent phylogenetic origins of methanotrophic and chemoautotrophic bacterial endosymbioses in marine bivalves. J Bacteriol 176 : 1932 1938.
19. Distel, D.L., Lane, D., Olsen, G., Giovannoni, S., Pace, B., Stahl, D. Felbeck, H. (1988) Sulfur-oxidizing bacterial endosymbionts - analysis of phylogeny and specificity by 16S ribosomal RNA sequences. J Bacteriol 170 : 2506 2510.
20. Distel, D.L., Lee, H.K.W. Cavanaugh, C.M. (1995) Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc Natl Acad Sci USA 92 : 9598 9602.
21. Distel, D.L., Baco, A., Chuang, E., Morrill, W., Cavanaugh, C. Smith, C. (2000) Do mussels take wooden steps to deep-sea vents? Nature 403 : 725 726.
22. Duperron, S., Nadalig, T., Caprais, J.C., Sibuet, M., Fiala-Médioni, A., Amann, R. Dubilier, N. (2005) Dual symbiosis in a Bathymodiolus mussel from a methane seep on the Gabon continental margin (South East Atlantic): 16S rRNA phylogeny and distribution of the symbionts in the gills. Appl Environ Microbiol 71 : 1694 1700.
23. Duperron, S., Bergin, C., Zielinski, F., McKiness, Z.P., DeChaine, E.G., Cavanaugh, C.M. Dubilier, N. (2006) A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and B. puteoserpentis (Bivalvia: Mytilidae), from hydrothemal vents along the northern Mid-Atlantic Ridge. Environ Microbiol 8 : 1441 1447.
24. Duperron, S., Sibuet, M., MacGregor, B.J., Kuypers, M.M., Fisher, C.R. Dubilier, N. (2007a) Diversity, relative abundance, and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussels (Bivalvia: Mytilidae) from cold seeps in the Gulf of Mexico. Environ Microbiol 9 : 1423 1438.
25. Duperron, S., Fiala-Médioni, A., Caprais, J.C., Olu, K. Sibuet, M. (2007b) Evidence for chemoautotrophic symbiosis in a Mediterranean cold seep clam (Bivalvia: Lucinidae): comparative sequence analysis of bacterial 16S rRNA, APS reductase and RubisCO genes. FEMS Microbiol Ecol 59 : 64 70.
26. Elsaied, H.E., Kaneko, R. Naganuma, T. (2006) Molecular characterization of a deep-sea methanotrophic mussel symbiont that carries a RuBisCO gene. Mar Biotechnol 8 : 511 520.
27. Fiala-Médioni, A., McKiness, Z.P., Dando, P., Boulegue, J., Mariotti, A., Alayse-Danet, A.M., et al. (2002) Ultrastructural, biochemical and immunological characterisation of two populations of he Mytilid mussel Bathymodiolus azoricus from the Mid Atlantic Ridge: evidence for a dual symbiosis. Mar Biotechnol 141 : 1035 1043.
28. Fisher, C.R. (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2 : 399 613.
29. Fisher, C.R., Childress, J.J., Oremland, R.S. Bidigare, R.R. (1987) The importance of methane and thiosulphate in the metabolism of the bacterial symbionts of two deep-sea mussels. Mar Biotechnol 96 : 59 71.
30. Fisher, C.R., Brooks, J.M., Vodenichar, J.S., Zande, J.M., Childress, J.J. Burke, R.A. Jr (1993) The co-occurrence of methanotrophic and chemoautotrophic sulfur oxydixing bacterial symbionts in a deep-sea mussel. PSZNI: Mar Ecol 14 : 277 289.
31. Folmer, O., Black, M.B., Hoeh, W.R., Lutz, R.A. Vrijenhoek, R.C. (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from metazoan invertebrates. Mol Mar Biol Biotechnol 3 : 294 299.
32. Fujiwara, Y., Takai, K., Uematsu, K., Tsuchida, S., Hunt, J.C. Hashimoto, J. (2000) Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels: influence on host distribution. Mar Ecol Prog Ser 208 : 147 155.
33. Gelman, A. Rubin, D. (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7 : 817 818.
34. Gosink, J.J., Woese, C.R. Staley, J.T. (1998) Polaribacter Gen. nov. with three new species, P. irgensii sp. nov., P. franzmannii sp. nov. & P. filamentus sp. nov., gas vacuolate polar marine bacteria of the Cytophaga-Flavobacterium-Bacteroides groups and reclassification of 'Flectobacillus glomeratus' as Polaribacter glomeratus comb. nov. Int J Syst Bacteriol 48 : 223 235.
35. Gustafson, R., Turner, R., Lutz, R. Vrijenhoek, R. (1998) A new genus and five new species of mussels (Bivavlia, Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40 : 63 112.
36. Hipp, W.M., Pott, A.S., Thum-Schmitz, N., Faath, I., Dahl, C. Truper, H. (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfide-oxidizing prokaryotes. Microbiology 143 : 2891 2902.
37. Horn, M., Harzeneter, M., Linner, T., Scmid, E.N., Müller, K.D., Michel, R. Wagner, M. (2001) Members of the Cutophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria in acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus'. Environ Microbiol 3 : 440 449.
38. Huber, T., Faulkner, G. Hugenholtz, P. (2004) Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20 : 2317 2319.
39. Hurst, G.D., Bandi, C., Sacchi, L., Cochrane, A.G., Betrtrand, D., Karaca, I. Majerus, M.E. (1999) Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited flavobacteria that kill males only. Parasitology 118 : 125 134.
40. Iwasaki, H., Kyuno, A., Shintaki, M., Fujita, Y., Fujiwara, Y., Fujikura, K., et al. (2006) Evolutionary relationships of deep-sea mussels inferred by mitochondrial DNA sequences. Mar Biotechnol 149 : 1111 1122.
41. Jones, W.J., Won, Y.J., Maas, P.A.Y., Smith, P.J., Lutz, R.A. Vrijenhoek, R.C. (2006) Evolution of habitat use by deep-sea mussels. Mar Bio 148 : 841 851.
42. Losekann, T., Knittel, K., Nadalig, T., Fuchs, B., Niemann, H., Boetius, A. Amann, R. (2007) Diversity and abundance of aerobic and anaerobic methane oxidizes at the haakon mosby mud volcano, barents sea. Appl Environ Microbiol 73 : 3348 3362.
43. MacAvoy, S.E., Macko, S.A. Joye, S.B. (2002) Fatty acid carbon isotope signatures in chemosynthetic mussels and tubeworms from Gulf of Mexico hydrocarbon seep communities. Chem Geol 185 : 1 8.
44. Madigan, M.T., Martinko, J.M. Parker, J. (2002) Brock Biology of Microorganisms. Upper Saddle River, NJ, USA : Pearson Education.
45. Manz, W., Amann, R., Ludwig, W., Vancanneyt, M. Schleifer, K.H. (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology 142 : 1097 1106.
46. Ohkuma, M., Noda, S., Hongoh, Y. Kudo, T. (2002) Diverse bacteria related to the Bacteroides subgroup of the CFB phylum within the gut symbiotic communities of various termites. Biosci Biotechnol Biochem 66 : 78 84.
47. Olu-LeRoy, K., Sibuet, M., Fiala-Médioni, A., Gofas, S., Salas, C., Mariotti, A., et al. (2004) Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis, and spatial distribution on mud volcanoes. Deep Sea Res I 51 : 1915 1936.
48. Pailleret, M., Haga, T., Petit, P., Privé-Gill, C., Saedlou, N., Gaill, F. Zbinden, M. (2007) Sunken woods from the Vanuatu islands: identification of wood substrates and preliminary description of associated fauna. Mar Ecol 27 : 1 9.
49. Peek, A.S., Feldman, R.A., Lutz, R.A. Vrijenhoek, R.C. (1998) Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc Natl Acad Sci USA 95 : 9962 9966.
50. Posada, D. Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14 : 817 818.
51. Qiu, X., Wu, L., Huang, H., McDonel, P., Palumbo, A.V., Tiedje, J.M. Zhou, J. (2001) Evaluation of PCR-generated chimaeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl Environ Microbiol 67 : 880 887.
52. Ronquist, F. Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 : 1572 1574.
53. Schwedock, J., Hermer, T.L., Scott, K.M., Hektor, H.J., Seitz, A.P. Fontana, M.C., et al. (2004) Characterization and expression of genes from the RubisCO gene cluster of the chemoautotrophic symbiont of Solemya velum: cbbLSQO. Arch Microbiol 182 : 18 29.
54. Spiridonova, E.M., Kuznetsov, B.B., Pimenov, N.V. Tourova, T.P. (2006) Phylogenetic characterization of endosymbionts of the hydrothermal vents mussel Bathymodiolus azoricus by analysis of the 16S rRNA, cbbL, and pmoA genes. Microbiology 75 : 798 806.
55. Stewart, F.J., Newton, L.G. Cavanaugh, C.M. (2005) Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces. Trends Microbiol 13 : 439 448.
56. Suzuki, M.T., Preston, C.M., Beja, O., de le Torre, J.R., Steward, G.F. DeLong, E.F. (2004) Phylogenetic screening of ribosomal RNA gene-containing clones from Bacterial Artificial Chromosome (BAC) libraries from different depths in Monterey Bay. Microb Ecol 48 : 473 488.
57. Trask, J.L. Van Dover, C.L. (1999) Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol Oceanogr 44 : 334 343.
58. Uchino, Y. Yokota, A. (2003) 'Green-like' and 'Red-like' RubisCO cbbL genes in Rhodobacter azotoformans. Mol Biol Evol 20 : 821 830.
59. Von Cosel, R. (2002) A new species of bathymodioline mussel (Mollusca, Bivalvia, Mytilidae) from Mauritania (West Africa), with comments on the genus Bathymodiolus Kenk & Wilson, 1985. Zoosystema 24 : 259 271.
60. Ward, N., Larsen, O., Sakwa, J., Bruseth, L., Khouri, H., Durkin, A.S., et al. (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2 : E303.
61. Won, Y.J., Hallam, S.J., O'Mullan, D., Pan, I.L., Buck, K.R. Vrijenhoek, R.C. (2003) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl Environ Microbiol 69 : 6785 6792.