Phylogenetic characterization of episymbiotic bacteria hosted by a hydrothermal vent limpet (lepetodrilidae, vetigastropoda)

Biological Bulletin

Volumn 220, Issue 2, 2011, Pages 118-127

  Bates, Amanda E ^a   Harmer, Tara L ^b   Roeselers, Guus ^c   Cavanaugh, Colleen M ^c  

^a UNIVERSITY OF VICTORIA   (Canada)

^b RICHARD STOCKTON COLLEGE OF NEW JERSEY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPARATIVE STUDY; DEEP-SEA BENTHOS; HYDROTHERMAL VENT; MARINE ENVIRONMENT; MORPHOLOGY; PHYLOGENETICS; SNAIL; SYMBIONT; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; INVERTEBRATA; LEPETODRILIDAE; LEPETODRILUS FUCENSIS; MOLLUSCA; PATELLIDAE; PROTEOBACTERIA; VETIGASTROPODA;

EID: 79956337646     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv220n2p118     Document Type: Article

References (58)

1. Alayse-Danet, A. M., D. Desbruyères, and F. Gaill. 1987. The possible nutritional or detoxification role of the epibiotic bacteria of Alvinellid polychaetes: review of current data. Symbiosis 4: 51-62.
2. Amann, R. I. 1995. Fluorescently labeled, ribosomal-RNA-targeted oligonucleotide probes in the study of microbial ecology. Mol. Ecol. 4: 543-553.
3. Bates, A. E. 2007a. Feeding strategy, morphological specialization and the presence of bacterial symbionts in lepetodrilid gastropods from hydrothermal vents. Mar. Ecol. Prog. Ser. 347: 87-99.
4. Bates, A. E. 2007b. Persistence, morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux. Mar. Biol. 152: 557-568.
5. Bates, A. E., V. Tunnicliffe, and R. W. Lee. 2005. Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Mar. Ecol. Prog. Ser. 305: 1-15.
6. Behrens, S., B. M. Fuchs, F. Mueller, and R. Amann. 2003. Is the in situ accessibility of the 16S rRNA of Escherichia coli for Cy3-labeled oligonucleotide probes predicted by a three-dimensional structure model of the 30S ribosomal subunit? Appl. Environ. Microbiol. 69: 4935-4941.
7. Blazejak, A., C. Erséus, R. Amann, and N. Dubilier. 2005. Coexistence of bacterial sulfide-oxidizers, sulfate-reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71: 1553-1561.
8. Cavanaugh, C. M. 1994. Microbial symbiosis: patterns of diversity in the marine environment. Am. Zool. 34: 79-89.
9. Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch, and J. B. Waterbury. 1981. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213: 340-342.
10. Cavanaugh, C. M., Z. P. McKiness, I. L. G. Newton, and F. J. Stewart. 2006. Marine chemosynthetic symbioses. Pp. 475-507 in The Pro-karyotes, M. Dworkin, S. I. Falkow, E. Rosenberg, K. H. Schleifer, and E. Stackebrandt, eds. Springer, New York.
11. Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, T. Marsh, G. M. Garrity, and J. M. Tiedje. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37(suppl. 1): D141-D145.
12. Dattagupta, S., I. Schaperdoth, A. Montanari, S. Mariani, N. Kita, J. W. Valley, and J. L. Macalad. 2009. A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. ISME J. 8: 935-943.
13. de Burgh, M. E., and C. L. Singla. 1984. Bacterial colonization and endocytosis on the gill of a new limpet species from a hydrothermal vent. Mar. Biol. 84: 1-6.
14. DeChaine, E. G., and C. M. Cavanaugh. 2005. Symbioses of methanotrophs and deep-sea mussels (Mytilidae: Bathymodiolinae). Pp. 227-249 in Molecular Basis of Symbiosis, J. Overmann, ed. Springer-Verlag, Berlin.
15. DeChaine, E. G., A. E. Bates, T. M. Shank, and C. M. Cavanaugh. 2006. Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ. Microbiol. 8: 1902-1912.
16. Di Meo-Savoie, C. A., G. W. Luther, and S. C. Cary. 2004. Physicochemical characterization of the microhabitat of the epibionts associated with Alvinella pompejana, a hydrothermal vent annelid. Geochim. Cosmochim. Acta 68: 2055-2066.
17. Dubilier, N., C. Mulders, T. Ferdelman, D. de Beer, A. Pernthaler, M. Klein, M. Wagner, C. Erseus, F. Thiermann, J. Krieger, et al. 2001. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411: 298-302.
18. Dubilier, N., C. Bergin, and C. Lott. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6: 725-740.
19. Dufour, S. 2005. Gill anatomy and the evolution of symbiosis in the bivalve family Thyasiridae. Biol. Bull. 208: 200-212.
20. Duperron, S., M. C. Laurent, F. Gaill, and O. Gros. 2008a. Sulfuroxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol. Ecol. 62: 338-349.
21. Duperron, S., S. Halary, J. Lorion, S. Myriam, and G. Francoise. 2008b. Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ. Microbiol. 10: 433-445.
22. Durand, L., M. Zbinden, V. Cueff-Gauchard, S. Duperron, E. Roussel, B. Shillito, and M. A. Cambon-Bonavita. 2010. Microbial diversity associated with the hydrothermal vent shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol. Ecol. 71: 291-303.
23. Felbeck, H., J. J. Childress, and G. N. Somero. 1981. Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature 292: 291-293.
24. Fox, M., S. K. Juniper, and H. Vali. 2002. Chemoautotrophy as a possible nutritional source in the hydrothermal vent limpet Lepetodrilus fucensis. Cah. Biol. Mar. 43: 371-376.
25. Goffredi, S. K., A. Warén, V. J. Orphan, C. L. V. Dover, and R. C. Vrijenhoek. 2004. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70: 3082-3090.
26. Goffredi, S. K., W. J. Jones, H. Erhlich, A. Springer, and R. C. Vrijenhoek. 2008. Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ. Microbiol. 10: 2623-2634.
27. Grzymski, J. J., A. E. Murray, B. J. Campbell, M. Kaplarevic, G. R. Gao, C. Lee, R. Daniel, A. Ghadiri, R. A. Feldman, and S. C. Cary. 2008. Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility. Proc. Natl. Acad. Sci. USA 105: 17516-17521.
28. Haddad, A., F. Camacho, P. Durand, and S. C. Cary. 1995. Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl. Environ. Microbiol. 61: 1679-1687.
29. Harmer, T. L., R. D. Rotjan, A. D. Nussbaumer, M. Bright, A. W. Ng, E. G. DeChaine, and C. M. Cavanaugh. 2008. Free-living tube worm endosymbionts found at deep-sea vents. Appl. Environ. Microbiol. 74: 3895-3898.
30. Hurtado, L. A., M. Mateos, R. A. Lutz, and R. C. Vrijenhoek. 2003. Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl. Environ. Microbiol. 69: 2058-2064.
31. Kadar, E., R. Bettencourt, V. Costa, R. Serrao Santos, A. Lobo-da Cunha, and P. Dando. 2005. Experimentally induced endosymbiont loss and reacquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. J. Exp. Mar. Biol. Ecol. 318: 99-110.
32. Katz, S., C. M. Cavanaugh, and M. Bright. 2006. Symbiosis of epiand endocuticular bacteria with Helicoradomenia spp. (Mollusca, Aplacophora, Solenogastres) from deep-sea hydrothermal vents. Mar. Ecol. Prog. Ser. 320: 89-99.
33. Lane, D. J. 1991. 16S/23S rRNA sequencing. Pp. 115-175 in Nucleic Acid Techniques in Bacterial Systematics, E. Stackebrandt and M. Goodfellow, eds. John Wiley, New York.
34. Levesque, C., K. S. Juniper, and H. Limen. 2006. Spatial organization of food webs along habitat gradients at deep-sea hydrothermal vents on Axial Volcano, Northeast Pacific. Deep Sea Res. I 53:726-739.
35. López-García, P., F. Gaill, and D. Moreira. 2002. Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environ. Microbiol. 4: 204-215.
36. Lösekann, T., A. Robador, H. Niemann, K. Knittel, A. Boetius, and N. Dubilier. 2008. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic Cold Seep (Haakon Mosby Mud Volcano, Barents Sea). Environ. Microbiol. 10: 3237-3254.
37. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, R. Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32: 1363-1371.
38. Luyten, Y. A., J. R. Thompson, W. Morrill, M. F. Polz, and D. L. Distel. 2006. Extensive variation in intracellular symbiont community composition among members of a single population of the woodboring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl. Environ. Microbiol. 72: 412-417.
39. McMullin, E. R., S. Hourdez, S. W. Schaeffer, and C. R. Fisher. 2003. Phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34:1-41.
40. Naganuma, T., C. Kato, H. Hirayama, N. Moriyama, J. Hashimoto, and K. Horikoshi. 1997. Intracellular occurrence of e-proteobacterial 16S rDNA sequences in the vestimentiferan trophosome. J. Oceanogr. 53: 193-197.
41. Petersen, J. M., A. Ramette, C. Lott, M. A. Cambon-Bonavita, M. Zbinden, and N. Dubilier. 2010. Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilon-proteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ. Microbiol. 12: 2204-2218.
42. Polz, M. F., and C. M. Cavanaugh. 1995. Dominance of one bacterial OTU at a Mid-Atlantic Ridge hydrothermal vent site. Proc. Natl. Acad. Sci. USA 92: 7232-7236.
43. Polz, M. F., D. L. Distel, B. Zarda, R. Amann, H. Felbeck, J. A. Ott, and C. M. Cavanaugh. 1994. Phylogenetic analysis of a highly specific association between ectosymbiotic, sulfur-oxidizing bacteria and a marine nematode. Am. Soc. Microbiol. 60: 4461-4467.
44. Polz, M. F., J. J. Robinson, C. M. Cavanaugh, and C. L. van Dover. 1998. Trophic ecology of massive shrimp aggregations at a Mid- Atlantic Ridge hydrothermal vent site. Limnol. Oceanogr. 43: 1631-1638.
45. Pruesse, E., C. Quast, K. Knittel, B. M. Fuchs, W. G. Ludwig, J. Peplies, and F. O. Glockner. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35: 7188-7196.
46. Riou, V., S. Duperron, S. Halary, E. Dehairs, S. Bouillon, I. Martins, A. Colac ̧o, and R. Serra ̃o Santos. 2010. Variation in physiological indicators in Bathymodiolus azoricus (Bivalvia: Mytilidae) at the Menez Gwen Mid-Atlantic Ridge deep-sea hydrothermal vent site within a year. Mar. Environ. Res. 70: 264-271.
47. Robidart, J. C., S. R. Bench, R. A. Feldman, A. Novoradovsky, S. B. Podell, T. Gaasterland, E. E. Allen, and H. Felbeck. 2008. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10: 727-737.
48. Ruehland, C., A. Blazejak, C. Lott, A. Loy, C. Erséus, and N. Dubilier. 2008. Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments. Environ. Microbiol. 10: 3404-3416.
49. Sambrook, J., and D. W. Russell. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
50. Southward, E. 2008. The morphology of bacterial symbioses in the gills of mussels of the genera Adipicola and Idas (Bivalvia: Mytilidae) J. Shellfish Res. 27: 139-146.
51. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57: 758-771.
52. Stewart, F. J., and C. M. Cavanaugh. 2009. Pyrosequencing analysis of endosymbiont population structure: co-occurrence of divergent symbiont lineages in a single vesicomyid host clam. Environ. Microbiol. 11: 2136-2147.
53. Suzuki, Y., T. Sasaki, M. Suzuki, S. Tsuchida, K. H. Nealson, and K. Horikoshi. 2006. Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: the genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol. Lett. 249: 105-112.
54. Taylor, J. D., and E. A. Glover. 2006. Lucinidae (Bivalvia)-the most diverse group of chemosymbiotic molluscs. Zool. J. Linn. Soc. 148: 421-438.
55. Urakawa, H., N. Dubilier, Y. Fujiwara, D. E. Cunningham, S. Kojima, and D. A. Stahl. 2005. Hydrothermal vent gastropods from the same family (Provannidae) harbour δ- and ε-proteobacterial endosymbionts. Environ. Microbiol. 7: 750-755.
56. Won, Y. J., S. Hallman, G. D. O'Mullan, I. L. Pan, K. R. Buck, and R. C. Vrijenhoek. 2003. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl. Environ. Microbiol. 69: 6785-6792.
57. Woyke, T., H. Teeling, N. M. Ivanova, M. Huntemann, M. Richter, F. O. Gloeckner, D. Boffelli, I. J. Anderson, K. W. Barry, H. J. Shapiro, et al. 2006. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
58. Zbinden, M., B. Shillito, N. Le Bris, C. de Villardi de Montlaur, E. Roussel, F. Guyot, F. Gaill, and M. Cambon Bonavita. 2008. New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J. Exp. Mar. Biol. Ecol. 359: 131-140.