The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: An in-depth metagenomic investigation and discovery of Zetaproteobacteria

Environmental Microbiology

Volumn 16, Issue 9, 2014, Pages 2723-2738

  Jan, Cyrielle ^a   Petersen, Jillian M ^b   Werner, Johannes ^b,c   Teeling, Hanno ^b   Huang, Sixing ^b   Glöckner, Frank Oliver ^b,c   Golyshina, Olga V ^d   Dubilier, Nicole ^b   Golyshin, Peter N ^d   Jebbar, Mohamed ^a   Cambon Bonavita, Marie Anne ^e  

^a Centre National de la Recherche Scientifique   (France)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c JACOBS UNIVERSITY BREMEN   (Germany)

^d BANGOR UNIVERSITY   (United Kingdom)

^e IFREMER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); DECAPODA (CRUSTACEA); EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; INVERTEBRATA; RIMICARIS EXOCULATA;

BACTERIAL DNA; RNA 16S;

ANIMAL; CARBON CYCLE; CHEMOAUTOTROPHY; DECAPODA (CRUSTACEA); DNA SEQUENCE; EPSILONPROTEOBACTERIA; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENETICS; GILL; HYDROTHERMAL VENT; METABOLISM; METAGENOMICS; MICROBIOLOGY; PHOTOSYNTHESIS; SYMBIOSIS;

ANIMALS; CARBON CYCLE; CHEMOAUTOTROPHIC GROWTH; DECAPODA (CRUSTACEA); DNA, BACTERIAL; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GILLS; HYDROTHERMAL VENTS; IN SITU HYBRIDIZATION, FLUORESCENCE; METAGENOMICS; PHOTOSYNTHESIS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84906943759     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12406     Document Type: Article

References (74)

1. Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R., and Stahl, D.A. (1990) Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial-populations. Appl Environ Microbiol 56: 1919-1925.
2. Aziz, R., Bartels, D., Best, A., DeJongh, M., Disz, T., Edwards, R., etal. (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
3. 2 acquisition by the CBB cycle. J Exp Bot 59: 1525-1541.
4. 2 fixation pathways. App Environ Microbiol 77: 1925-1936.
5. Campbell, B.J., and Cary, S.C. (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl Environ Microbiol 70: 6282-6289.
6. Campbell, B.J., Engel, A.S., Porter, M.L., and Takai, K. (2006) The versatile Epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Micro 4: 458-468.
7. Cavanaugh, C.M., McKiness, Z.P., Newton, I.L.G., and Stewart, F.J. (2006) The Prokaryotes: A Handbook on the Biology of Bacteria. New York, NY, USA: Springer.
8. 4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14 ' N, MAR). Chem Geol 191: 345-359.
9. 4 and abiotic hydrocarbons in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge. Geoch Cosmochim Acta 74: A163-A163.
10. Corbari, L., Zbinden, M., Cambon-Bonavita, M.A., Gaill, F., and Compere, P. (2008a) Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aqua Biol 1: 225-238.
11. Corbari, L., Cambon-Bonavita, M.A., Long, G.J., Grandjean, F., Zbinden, M., Gaill, F., etal. (2008b) Iron oxide deposits associated with the ectosymbiotic bacteria in the hydrothermal vent shrimp Rimicaris exoculata. Biogeosciences 5: 1295-1310.
12. Danese, P.N., Pratt, L.A., and Kolter, R. (2000) Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182: 3593-3596.
13. Dell, A., Galadar, A., Sastre, F., and Hitchen, P. (2010) Similarities and differences in the glycosylation mechanisms in prokaryotes and eucaryotes. Int J Microbiol 2010: 148178. doi:10.1155/2010/148178.
14. Dubilier, N., Bergin, C., and Lott, C. (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Micro 6: 725-740.
15. Duperron, S., Sibuet, M., MacGregor, B.J., Kuypers, M.M.M., Fisher, C.R., and Dubilier, N. (2007) Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ Microbiol 9: 1423-1438.
16. Duperron, S., Halary, S., Lorion, J., Sibuet, M., and Gaill, F. (2008) Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ Microbiol 10: 433-445.
17. Durand, É., Bernadac, A., Ball, G., Lazdunski, A., Sturgis, J.N., and Filloux, A. (2003) Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J Bacteriol 185: 2749-2758.
18. Durand, L., Zbinden, M., Cueff-Gauchard, V., Duperron, S., Roussel, E.G., Shillito, B., etal. (2010) Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol Ecol 71: 291-303.
19. Emerson, D., Rentz, J.A., Lilburn, T.G., Davis, R.E., Aldrich, H., Chan, C., etal. (2007) A novel lineage of Proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE 2: e667.
20. Ferrer, M., Guazzaroni, M.-E., Richter, M., García-Salamanca, A., Yarza, P., Suárez-Suárez, A., etal. (2011) Taxonomic and functional metagenomic profiling of the microbial community in the anoxic sediment of a sub-saline shallow lake (Laguna de Carrizo, Central Spain). Micro Ecol 62: 824-837.
21. Ferrer, M., Werner, J., Chernikova, T.N., Bargiela, R., Fernández, L., La Cono, V., etal. (2012) Unveiling microbial life in the new deep-sea hypersaline lake Thetis. Part II: a metagenomic study. Environ Microbiol 14: 268-281.
22. Friedrich, C.G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67: 2873-2882.
23. Grabovich, M.Y., Muntyan, M.S., Lebedeva, V.Y., Ustiyan, V.S., and Dubinina, G.A. (1999) Lithoheterotrophic growth and electron transfer chain components of the filamentous gliding bacterium Leucothrix mucor DSM 2157 during oxidation of sulfur compounds. FEMS Microbiol Lett 178: 155-161.
24. Grimm, F., Dobler, N., and Dahl, C. (2010) Regulation of dsr genes encoding proteins responsible for the oxidation of stored sulfur in Allochromatium vinosum. Microbiol 156: 764-773.
25. Grote, J., Schott, T., Bruckner, C.G., Glöckner, F.O., Jost, G., Teeling, H., etal. (2012) Genome and physiology of a model epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. Proc Natl Acad Sci USA 109: 506-510.
26. Guri, M., Durand, L., Cueff-Gauchard, V., Zbinden, M., Crassous, P., Shillito, B., etal. (2012) Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. ISME J 6: 597-609.
27. Heisterkamp, I.M., Schramm, A., Larsen, L.H., Svenningsen, N.B., Lavik, G., de Beer, D., etal. (2012) Shell biofilm-associated nitrous oxide production in marine molluscs: processes, precursors and relative importance. Environ Microbiol 15: 1943-1955.
28. Hensen, D., Sperling, D., Trüper, H.G., Brune, D.C., and Dahl, C. (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62: 794-810.
29. Hügler, M., Petersen, J.M., Dubilier, N., Imhoff, J.F., and Sievert, S.M. (2011) Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS ONE 6: e16018.
30. Inagaki, F., Takai, K., Kobayashi, H., Nealson, K.H., and Horikoshi, K. (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ε-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53: 1801-1805.
31. Inagaki, F., Takai, K., Nealson, K.H., and Horikoshi, K. (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the ε-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54: 1477-1482.
32. Kato, S., Yanagawa, K., Sunamura, M., Takano, Y., Ishibashi, J., Kakegawa, T., etal. (2009) Abundance of Zetaproteobacteria within crustal fluids in back-arc hydrothermal fields of the Southern Mariana Trough. EnvironMicrobiol 11: 3210-3222.
33. Kornberg, A. (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177: 491-496.
34. Kulajta, C., Thumfart, J.O., Haid, S., Daldal, F., and Koch, H.-G. (2006) Multi-step assembly pathway of the cbb3-type cytochrome c oxidase complex. J Mol Biol 355: 989-1004.
35. Macalady, J.L., Dattagupta, S., Schaperdoth, I., Jones, D.S., Druschel, G.K., and Eastman, D. (2008) Niche differentiation among sulfur-oxidizing bacterial populations in cave waters. ISME J 2: 590-601.
36. Markert, S., Arndt, C., Felbeck, H., Becher, D., Sievert, S.M., Hügler, M., etal. (2007) Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315: 247-250.
37. Meyer, F., Goesmann, A., McHardy, A.C., Bartels, D., Bekel, T., Clausen, J., etal. (2003) GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31: 2187-2195.
38. Nakagawa, S., Takai, K., Inagaki, F., Hirayama, H., Nunoura, T., Horikoshi, K., etal. (2005) Distribution, phylogenetic diversity and physiological characteristics of ε-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7: 1619-1632.
39. Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A.L., Takai, K., and Horikoshi, K. (2007) Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104: 12146-12150.
40. Petersen, J.M., Ramette, A., Lott, C., Cambon-Bonavita, M.A., Zbinden, M., and Dubilier, N. (2010) Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous Gamma- and Epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ Microbiol 12: 2204-2218.
41. Petersen, J.M., Zielinski, F.U., Pape, T., Seifert, R., Moraru, C., Amann, R., etal. (2011) Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476: 176-180.
42. Pitcher, R.S., and Watmough, N.J. (2004) The bacterial cytochrome cbb3 oxidases. BBA - Bioenergetics 1655: 388-399.
43. Polz, M.F., Robinson, J.J., Cavanaugh, C.M., and Van Dover, C.L. (1998) Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnol Oceanograph 43: 1631-1638.
44. Ponsard, J., Cambon-Bonavita, M.-A., Zbinden, M., Lepoint, G., Joassin, A., Corbari, L., etal. (2013) Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. ISME J 7: 96-109.
45. Powell, M.A., and Somero, G.N. (1986) Adaptation to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biol Bull 171: 274-290.
46. Prosser, J.I. (2012) Ecosystem processes and interactions in a morass of diversity. FEMS Microbiol Ecol 81: 507-519.
47. Raggi, L., Schubotz, F., Hinrichs, K.U., Dubilier, N., and Petersen, J.M. (2013) Bacterial symbionts of Bathymodiolus mussels and Escarpia tubeworms from Chapopote, an asphalt seep in the southern Gulf of Mexico. Environ Microbiol 15: 1969-1987.
48. Ravaux, J., Gaill, F., Le Bris, N., Sarradin, P.M., Jollivet, D., and Shillito, B. (2003) Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J Exp Biol 206: 2345-2354.
49. Ravaux, J., Toullec, J.Y., Leger, N., Lopez, P., Gaill, F., and Shillito, B. (2007) First hsp70 from two hydrothermal vent shrimps, Mirocaris fortunata and Rimicaris exoculata: characterization and sequence analysis. Gene 386: 162-172.
50. Richter, M., Lombardot, T., Kostadinov, I., Kottmann, R., Duhaime, M., Peplies, J., etal. (2008) JCoast - A biologist-centric software tool for data mining and comparison of prokaryotic (meta)genomes. BMC Bioinformatics 9: 177.
51. Schmidt, C., Le Bris, N., and Gaill, F. (2008) Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J Shellfish Res 27: 79-90.
52. Schmidt, C., Corbari, L., Gaill, F., and Le Bris, N. (2009) Biotic and abiotic controls on iron oxyhydroxide formation in the gill chamber of the hydrothermal vent shrimp Rimicaris exoculata. Geobiology 7: 454-464.
53. Sievert, S.M., Scott, K.M., Klotz, M.G., Chain, P.S.G., Hauser, L.J., Hemp, J., etal. (2008a) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74: 1145-1156.
54. Sievert, S.M., Hügler, M., Taylor, C.D., and Wirsen, C.O. (2008b) Sulfur oxidation at deep-sea hydrothermal vents. In Microbial Sulfur Metabolism. Christiane, D., and Cornelius, G.F. (eds.). Berlin, Heidelberg, Germany: Springer, pp. 238-258.
55. Singer, E., Emerson, D., Webb, E.A., Barco, R.A., Kuenen, J.G., Nelson, W.C., etal. (2011) Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe(II) oxidizing Zetaproteobacterium. PLoS ONE 6: e25386.
56. Szymanski, C.M., and Wren, B.W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Micro 3: 225-237.
57. Szymanski, C.M., Yao, R., Ewing, C.P., Trust, T.J., and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32: 1022-1030.
58. Takai, K., Nealson, K.H., and Horikoshi, K. (2004) Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the ε-Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. Int J Syst Evol Microbiol 54: 25-32.
59. Takai, K., Campbell, B.J., Cary, S.C., Suzuki, M., Oida, H., Nunoura, T., etal. (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microbiol 71: 7310-7320.
60. Takai, K., Suzuki, M., Nakagawa, S., Miyazaki, M., Suzuki, Y., Inagaki, F., etal. (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56: 1725-1733.
61. Thomas, T., Evans, F.F., Schleheck, D., Mai-Prochnow, A., Burke, C., Penesyan, A., etal. (2008) Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. PLoS ONE 3: e3252.
62. Troll, J.V., Adin, D.M., Wier, A.M., Paquette, N., Silverman, N., Goldman, W.E., etal. (2009) Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol 11: 1114-1127.
63. Vignais, P.M. (2008) Regulation of hydrogenase gene expression. In Govindjee, The Purple Phototrophic Bacteria. Hunter, C.N., Daldal, F., Thurnauer, M.C., and Beatty, J.T. (eds.). The Netherlands: Springer, pp. 743-757.
64. Vignais, P.M., and Colbeau, A. (2004) Molecular biology of microbial hydrogenases. Cur Iss Mol Biol 4: 159-188.
65. Whittaker, C.A., and Hynes, R.O. (2002) Distribution and evolution of von Willebrand/Integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13: 3369-3387.
66. Williams, A.B., and Rona, P.A. (1986) Two New Caridean Shrimps (Bresiliidae) From a Hydrothermal Field on the Mid-Atlantic Ridge, Vol. 6. San Antonio, TX, USA: Crustacean Society.
67. Wright, P.A. (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198: 273-281.
68. Yamamoto, M., and Takai, K. (2011) Sulfur metabolisms in epsilon- and gamma-proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2: 192-200.
69. Yamamoto, M., Nakagawa, S., Shimamura, S., Takai, K., and Horikoshi, K. (2010) Molecular characterization of inorganic sulfur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environ Microbiol 12: 1144-1153.
70. Yarzábal, A., Brasseur, G., Ratouchniak, J., Lund, K., Lemesle-Meunier, D., DeMoss, J.A., etal. (2002) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184: 313-317.
71. Zbinden, M., and Cambon-Bonavita, M.A. (2003) Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Ecol 46: 23-30.
72. Zbinden, M., Bris, N.L., Gaill, F., and Compère, P. (2004) Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Progr Series 284: 237-251.
73. Zbinden, M., Shillito, B., Le Bris, N., de Villardi de Montlaur, C., Roussel, E., Guyot, F., etal. (2008) New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J Experim Mar Biol Ecol 359: 131-140.
74. Zhu, F., Massana, R., Not, F., Marie, D., and Vaulot, D. (2005) Mapping of picoeukaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52: 79-92.