Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-Proteobacterial symbionts

Environmental Microbiology Reports

Volumn 6, Issue 6, 2014, Pages 656-664

  Beinart, R A ^a   Nyholm, S V ^b   Dubilier, N ^c   Girguis, P R ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALVINICONCHA; GASTROPODA; OCEANOSPIRILLALES; PROTEOBACTERIA;

ANIMAL; BIODIVERSITY; CLASSIFICATION; ENDOPHYTE; GAMMAPROTEOBACTERIA; GENETICS; GILL; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SNAIL; SYMBIOSIS;

ANIMALS; BIODIVERSITY; ENDOPHYTES; GAMMAPROTEOBACTERIA; GILLS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SNAILS; SYMBIOSIS;

EID: 84913546726     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12183     Document Type: Article

References (51)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Bio 215: 403-410.
2. Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R., and Stahl, D.A. (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925.
3. Bayer, T., Arif, C., Ferrier-Pagès, C., Zoccola, D., Aranda, M., and Voolstra, C.R. (2013a) Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar Ecol Prog Ser 479: 75-84.
4. Bayer, T., Neave, M.J., Alsheikh-Hussain, A., Aranda, M., Yum, L.K., Mincer, T. etal. (2013b) The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl Environ Microbiol 79: 4759-4762.
5. Beinart, R.A., Sanders, J.G., Faure, B., Sylva, S.P., Lee, R.W., Becker, E.L., etal. (2012) Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. PNAS 109: 19053-19054.
6. Bourne, D.G., and Munn, C.B. (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7: 1162-1174.
7. Bourne, D.G., Dennis, P.G., Uthicke, S., Soo, R.M., Tyson, G.W., and Webster, N. (2013) Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7: 1452-1458.
8. Casadevall, A. (2008) Evolution of intracellular pathogens. Annu Rev Microbiol 62: 19-33.
9. Cavanaugh, C., McKiness, Z., Newton, I., and Stewart, F. (2006) Marine chemosynthetic symbioses. In The Prokaryotes. Rosenberg, E., DeLong, E.F., Lory, S., and Stackebrandt, E., (eds). Berlin, Germany: Springer-Verlag, pp. 475-507.
10. Chen, M.H., Sheu, S.Y., Chen, C.A., Wang, J.T., and Chen, W.M. (2013) Corallomonas stylophorae gen. nov., sp. nov., a halophilic bacterium isolated from the reef-building coral Stylophora pistillata. Int J Syst Evol Microbiol 63: 982-988.
11. Costa, P.M., Carreira, S., Lobo, J., and Costa, M.H. (2012) Molecular detection of prokaryote and protozoan parasites in the commercial bivalve Ruditapes decussatus from southern Portugal. Aquaculture 370-371: 61-67.
12. Desbruyeres, D., Alaysedanet, A.M., Ohta, S., Antoine, E., Barbier, G., Briand, P., etal. (1994) Deep-sea hydrothermal communities in southwestern Pacific back-arc basins (The North Fiji and Lau Basins) - composition, microdistribution and food-web. Mar Geol 116: 227-242.
13. Dubilier, N., Bergin, C., and Lott, C. (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6: 725-740.
14. Endow, K., and Ohta, S. (1989) The symbiotic relationship between bacteria and a mesogastropod snail, Alviniconcha hessleri, collected from hydrothermal vents of the Mariana back-arc basin. Bull Jpn Soc Microb Ecol 3: 73-82.
15. Flemer, B., Kennedy, J., Margassery, L.M., Morrissey, J.P., O'Gara, F., Dobson, A.D.W. (2011) Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. J Appl Microbiol 112: 289-301.
16. ® of Systematic Bacteriology. Brenner, D.J., Krieg, N.R., Garrity, G.M., Boone, D.R., De Vos, P., etal. (eds). New York, NY, USA: Springer, pp. 270-323.
17. Goebel, W., and Gross, R. (2001) Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol 9: 267-273.
18. Goffredi, S.K., Orphan, V.J., Rouse, G.W., Jahnke, L., Embaye, T., Turk, K., etal. (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7: 1369-1378.
19. Goffredi, S.K., Yi, H., Zhang, Q., Klann, J.E., and Struve, I.A. (2014) Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms. ISME J 8: 908-924.
20. Henry, M.S., Childress, J.J., and Figueroa, D. (2008) Metabolic rates and thermal tolerances of chemoautotrophic symbioses from Lau Basin hydrothermal vents and their implications for species distributions. Deep Sea Res Part I: Oceanogr Res Pap 55: 679-695.
21. Jensen, S., Duperron, S., Birkeland, N-K., and Hovland, M. (2010) Intracellular Oceanospirillales bacteria inhabit gills of Acesta bivalves. FEMS Microbiol Ecol 74: 523-533.
22. Johnson, S.B., Warén, A., Lee, R.W., Kano, Y., Kaim, A., Davis, A., etal. (2010) Rubyspira, new genus and two new species of bone-eating deep-sea snails with ancient habits. Biol Bull 219: 166-177.
23. Kennedy, J., Codling, C.E., Jones, B.V., Dobson, A.D.W., and Marchesi, J.R. (2008) Diversity of microbes associated with the marine sponge, Haliclona simulans, isolated from Irish waters and identification of polyketide synthase genes from the sponge metagenome. Environ Microbiol 10: 1888-1902.
24. Kumar, Y., and Valdivia, R.H. (2009) Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5: 593-601.
25. Kurahashi, M., and Yokota, A. (2007) Endozoicomonas elysicola gen. nov., sp. nov., a γ-proteobacterium isolated from the sea slug Elysia ornata. Syst Appl Microbiol 30: 202-206.
26. La Rivière, M., Roumagnac, M., Garrabou, J., and Bally, M. (2013) Transient shifts in bacterial communities associated with the temperate Gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea. PLoS ONE 8: e57385.
27. Mira, A., and Moran, N.A. (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol 44: 137-143.
28. Nishijima, M., Adachi, K., Katsuta, A., Shizuri, Y., and Yamasato, K. (2013) Endozoicomonas numazuensis sp. nov., a gammaproteobacterium isolated from marine sponges, and emended description of the genus Endozoicomonas Kurahashi and Yokota 2007. Int J Syst Evol Microbiol 63: 709-714.
29. Oliver, K.M., Degnan, P.H., Burke, G.R., and Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
30. Podowski, E.L., Moore, T.S., Zelnio, K.A., Luther, G.W., and Fisher, C.R. (2009) Distribution of diffuse flow megafauna in two sites on the Eastern Lau Spreading Center, Tonga. Deep Sea Res Part I: Oceanogr Res Pap 56: 2041-2056.
31. Podowski, E.L., Ma, S., Luther, G.W., Wardrop, D., and Fisher, C.R. (2010) Biotic and abiotic factors affecting distributions of megafauna in diffuse flow on andesite and basalt along the Eastern Lau Spreading Center, Tonga. Mar Ecol Prog Ser 418: 25-45.
32. Raina, J.B., Tapiolas, D., Willis, B.L., and Bourne, D.G. (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75: 3492-3501.
33. Ramirez-Llodra, E., Shank, T.M., German, C.R. (2007) Biodiversity and biogeography of hydrothermal vent species thirty years of discovery and investigations. Oceanography 20: 30-41.
34. Sanders, J.G., Beinart, R.A., Stewart, F.J., DeLong, E.F., and Girguis, P.R. (2013) Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J 7: 1556-1567.
35. Santos-Garcia, D., Farnier, P.A., and Beitia, F. (2012) Complete genome sequence of 'Candidatus Portiera aleyrodidarum' BT-QVLC, an obligate symbiont that supplies amino acids and carotenoids to Bemisia tabaci. J Bacteriol 194: 6654-6655.
36. Smallcombe, A. (2001) Multicolor imaging: the important question of co-localization. Biotechniques 30: 1240-1246.
37. Stein, J.L., Cary, S.C., Hessler, R.R., Ohta, S., Vetter, R.D., Childress, J.J., and Felbeck, H. (1988) Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biol Bull 174: 373-378.
38. Sunagawa, S., Woodley, C.M., and Medina, M. (2010) Threatened corals provide underexplored microbial habitats. PLoS ONE 5: e9554.
39. Suzuki, Y., Sasaki, T., Suzuki, M., Nogi, Y., Miwa, T., Takai, K., etal. (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71: 5440-5450.
40. Suzuki, Y., Sasaki, T., Suzuki, M., Tsuchida, S., Nealson, K.H., and Horikoshi, K. (2005) Molecular phylogenetic and isotopic evidence of two lineages of chemo auto trophic endosymbionts distinct at the subdivision level harbored in one host-animal type: The genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol Lett 249: 105-112.
41. Suzuki, Y., Kojima, S., Sasaki, T., Suzuki, M., Utsumi, T., Watanabe, H., etal. (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72: 1388-1393.
42. Thao, M.L., and Baumann, P. (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70: 3401-3406.
43. Urakawa, H., Dubilier, N., Fujiwara, Y., Cunningham, D.E., Kojima, S., and Stahl, D.A. (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbour epsilon- and gamma-proteobacterial endosymbionts. Environ Microbiol 7: 750-754.
44. Van Alstyne, K.L., Dominique, V.J. III, and Muller-Parker, G. (2008) Is dimethylsulfoniopropionate (DMSP) produced by the symbionts or the host in an anemone-zooxanthella symbiosis? Coral Reefs 28: 167-176.
45. Van Dover, C.L., Humphris, S.E., Fornari, D., Cavanaugh, C.M., Collier, R., Goffredi, S.K., etal. (2001) Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294: 818-823.
46. Verna, C., Ramette, A., Wiklund, H., Dahlgren, T.G., Glover, A.G., Gaill, F., and Dubilier, N. (2010) High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environ Microbiol 12: 2355-2370.
47. Vonesch, C., and Unser, M. (2008) A fast thresholded landweber algorithm for wavelet-regularized multidimensional deconvolution. IEEE Trans Image Process 17: 539-549.
48. Wallner, G., Amann, R., and Beisker, W. (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136-143.
49. Yang, C.S., Chen, M.H., Arun, A.B., Chen, C.A., Wang, J.T., and Chen, W.M. (2010) Endozoicomonas montiporae sp. nov., isolated from the encrusting pore coral Montipora aequituberculata. Int J Syst Evol Microbiol 60: 1158-1162.
50. Zielinski, F.U., Pernthaler, A., Duperron, S., Raggi, L., Giere, O., Borowski, C., and Dubilier, N. (2009) Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ Microbiol 11: 1150-1167.
51. Zurel, D., Benayahu, Y., Or, A., Kovacs, A., and Gophna, U. (2011) Composition and dynamics of the gill microbiota of an invasive Indo-Pacific oyster in the eastern Mediterranean Sea. Environ Microbiol 13: 1467-1476.