New digestive symbiosis in the hydrothermal vent amphipoda Ventiella sulfuris

Comptes Rendus - Biologies

Volumn 335, Issue 2, 2012, Pages 142-154

  Corbari, Laure ^a   Durand, Lucile ^b   Cambon Bonavita, Marie Anne ^b   Gaill, Françoise ^c   Compère, Philippe ^d  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b Centre National de la Recherche Scientifique   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Amphipoda; Bacterial symbiosis; Hindgut; Hydrothermal vents; Midgut

Indexed keywords

RNA 16S;

AMPHIPOD; BACTERIUM; EPIBIONT; HYDROTHERMAL VENT; MICROBIAL COMMUNITY; MICROSCOPY; SYMBIOSIS;

AMPHIPODA; ARTICLE; DIGESTIVE FUNCTION; EPIBIONT; EPSILONPROTEOBACTERIA; HYDROTHERMAL VENT; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROSCOPY; NONHUMAN; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; VENTIELLA SULFURIS;

AMPHIPODA; ANIMALS; DIGESTIVE SYSTEM; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; SYMBIOSIS;

EAST PACIFIC RISE; PACIFIC OCEAN;

ALVINELLA POMPEJANA; ALVINELLIDAE; AMPHIPODA; BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; VENTIELLA SULFURIS;

EID: 84857040315     PISSN: 16310691     EISSN: 17683238     Source Type: Journal    
DOI: 10.1016/j.crvi.2011.12.005     Document Type: Article

References (70)

1. J.L. Barnard, and C. Ingram Lysianassoid Amphipoda (Crustacea) from deep-sea hydrothermal vents Smithsonian. Contrib. Zool. 499 1990 1 80
2. N. Vinogradov Amphipoda (Crustacea) from thermal vents in the Eastern Pacific Hydrobiol. J. 29 1993 77 92
3. D. Bellan-Santini Crustacés Amphipodes des sources hydrothermales: bilan des connaissances Cah. Biol. Mar. 39 1998 143 152 (Pubitemid 29429179)
4. K.L. Erickson, S.A. Macko, and C.L. Van Dover Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep-Sea Research Part II Top. Stud. Oceanograph. 56 2009 1577 1585
5. N. Vinogradov Amphipods from hydrothermal vents and cold seepings on the ocean bottom Oceanology 35 1995 69 74
6. B. Govenar, N. Le Bris, S. Gollner, J. Glanville, A. Aperghis, S. Hourdez, and C.R. Fisher Epifaunal community structure associated with Riftia pachyptila aggregations in chemically different hydrothermal vent habitats Mar. Ecol. Prog. Ser. 305 2005 67 77 (Pubitemid 43182295)
7. S. Galkin, and E. Goroslavskaya Bottom fauna associated with mussel beds and alvinellid communities in the hydrothermal field at 9° N of the East Pacific Rise Oceanology 48 2008 509 516
8. M. Sheader, C.L. Van Dover, and M. Thurston Reproductive ecology of Bouvierella curtirama (Amphipoda: Eusiridae) from chemically distinct vents in the Lucky Strike vent field, Mid-Atlantic Ridge Mar. Biol. 144 2004 503 514 (Pubitemid 38377577)
9. M. Sheader, and C.L. Van Dover Temporal and spatial variation in the reproductive ecology of the vent-endemic amphipod Ventiella sulfuris in the eastern Pacific Mar. Ecol. Prog. Ser. 331 2007 181 194 (Pubitemid 46408729)
10. J. Childress Life in sulfidic environments: historical perspective and current research trends Am. Zool. 35 1995 83 90
11. C. Cavanaugh, Z. McKiness, I. Newton, and F. Stewart Marine Chemosynthetic Symbioses M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt, The Prokaryotes 2006 Springer New-York 475 507
12. J. Ott, M. Bright, and S. Bulgheresi Marine Microbial Thiotrophic Ectosymbioses Oceanograph. Mar. Biol.: An Annual Review 42 2004 95 118 (Pubitemid 44568982)
13. N. Dubilier, C. Bergin, and C. Lott Symbiotic diversity in marine animals: the art of harnessing chemosynthesis Nat. Rev. Microbiol. 6 2008 725 740
14. S. Goffredi, A. Jones, H. Erhlich, A. Springer, and R. Vrijenhoek Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta Environ. Microbiol. 10 2008 2623 2634
15. S.K. Goffredi Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates Environ. Microbiol. Rep. 2 2010 479 488
16. R. Lemaitre Discovery of the first hermit crab (Crustacea: Decapoda: Parapaguridae) associated with hydrothermal vents Cah. Biol. Mar. 45 2004 325 334 (Pubitemid 40294887)
17. Y. Suzuki, M. Suzuki, S. Tsuchida, K. Takai, K. Horikoshi, A.J. Southward, W.A. Newman, and T. Yamaguchi Molecular investigations of the stalked barnacle Vulcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand J. Mar. Biol. Ass. U.K. 89 2009 727 733
18. C. Van Dover, B. Fry, F. Grassle, S. Humphris, and P.A. Rona Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge Mar. Biol. 98 1988 209 216
19. B. Casanova, M. Brunet, and M. Segonzac L'impact d'une épibiose bactérienne sur la morphologie fonctionnelle de crevettes associées à l'hydrothermalisme médio-Atlantique Cah. Biol. Mar. 34 1993 573 588 (Pubitemid 2049400)
20. M.F. Polz, and C.M. Cavanaugh Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site PNAS 92 1995 7232 7236
21. M. Zbinden, N. Le Bris, F. Gaill, and P. Compre Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes Mar. Ecol. Prog. Ser. 284 2004 237 251 (Pubitemid 40118218)
22. M. Zbinden, B. Shillito, N. Le Bris, C. de Villardi de Montlaur, E. Roussel, F. Guyot, F. Gaill, and M.-A. Cambon-Bonavita New insigths on the metabolic diversity among the epibiotic microbial communitiy of the hydrothermal shrimp Rimicaris exoculata J. Exp. Mar. Biol. Ecol. 359 2008 131 140
23. L. Corbari, M.-A. Cambon-Bonavita, M. Zbinden, F. Gaill, and P. Compre Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle Aquat. Biol. 1 2008 225 238
24. M. Zbinden, and M.-A. Cambon-Bonavita Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut FEMS Microbiol. Ecol. 46 2003 23 30 (Pubitemid 37297717)
25. L. Durand, M. Zbinden, V. Cueff-Gauchard, S. Duperron, E.G. Roussel, B. Shillito, and M.A. Cambon-Bonavita Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community FEMS Microbiol. Ecol. 71 2010 291 303
26. D.E. Bignell The arthropod gut as an environment for microorganisms J.M. Anderson, A.D.M. Rayner, D.W.H. Walton, Invertebrate-Microbial Interactions 1984 Cambridge University Press Cambridge 205 228
27. J. Harris The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis Microbiol. Ecol. 25 1993 195 231
28. D. Drobne Bacteria adherent to the hindgut of terrestrial isopods Acta Microbiologica Immunologica Hungarica 42 1995 45 52
29. S. Altschul, W. Gish, W. Miller, E. Myers, and D. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
30. N. Galtier, M. Gouy, and C. Gautier SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignement and molecular phylogeny CABIOS 12 1996 543 548
31. J. Felsentein Confidence limits on phylogenies: an approach using the bootstrap Evolution 30 1985 783 791
32. N. Saitou, and M. Nei The neighbor-joining method: a new method for reconstructing phylogenetic trees Mol. Biol. Evol. 4 1987 406 425
33. J.D. Icely, and J.A. Nott On the Morphology and Fine Structure of the Alimentary Canal of Corophium volutator (Pallas) (Crustacea: Amphipoda), Philosophical Transactions of the Royal Society of London. Series B Biol. Sci. 306 1984 49 78
34. M.D. Johnston, D.J. Johnston, and A.M.M. Richardson Differences in mouthpart and digestive tract structure between 4 ecologically distinct talitrid amphipods from Tasmania J. Mar. Biol. Assoc. U.K 84 2004 717 726 (Pubitemid 39234791)
35. L. Lepescheux Spatial organization of collagen in annelid cuticle: order and defects Biol Cell 62 1998 17 31
36. F. Gaill, and S. Hunt The biology of annelid worms from high temperature hydrothermal vent regions Rev. Aquat. Sci. 4 1991 107 137
37. L. Orrhage Light and electron microscope studies of some annelid setae Acta. Zoologica. 52 1971 157 169
38. S.Y. Al-Mohanna, and J.D. Nott B-cells and ingestion in the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) J. Mar. Biol. Assoc. U. K. 66 1986 403 414
39. K. Li, W. Guan, G. Wei, B. Liu, J. Xu, L. Zhao, and Y. Zhang Phylogenetic analysis of intestinal bacteria in the Chinese mitten crab (Eriocheir sinensis) J. Appl. Microbiol. 103 2007 675 682 (Pubitemid 47256339)
40. A.K. Dunn, and E.V. Stabb Culture-Independent Characterization of the Microbiota of the Ant Lion Myrmeleon mobilis (Neuroptera: Myrmeleontidae) Appl. Environ. Microbiol. 71 2005 8784 8794 (Pubitemid 41804015)
41. Y. Wang, A. Brune, and M. Zimmer Bacterial symbionts in the hepatopancreas of isopods: diversity and environmental transmission FEMS Microbiol. Ecol. 61 2007 141 152 (Pubitemid 46889832)
42. J.G. Mueller, R. Devereux, D.L. Santavy, S.E. Lantz, S.G. Willis, and P.H. Pritchard Phylogenetic and physiological comparisons of PAH-degrading bacteria from geographically diverse soils Antonie Van Leeuwenhoek 71 1997 329 343 (Pubitemid 27243738)
43. C.S. Lee, K.K. Kim, Z. Aslam, and S.-T. Lee Rhodanobacter thiooxydans sp. nov., isolated from a biofilm on sulfur particles used in an autotrophic denitrification process Int. J. Syst. Evol. Microbiol. 57 2007 1775 1779 (Pubitemid 47308411)
44. S.K. Goffredi, A. Waren, V.J. Orphan, C.L. Van Dover, and R.C. Vrijenhoek Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean Appl. Environ. Microbiol. 70 2004 3082 3090 (Pubitemid 38657827)
45. K. Alain, M. Olagnon, D.P.A. Desbruyres, G. Barbier, S.K. Juniper, J. Quérellou, and M.-A. Cambon-Bonavita Phylogenetic characterization of the bacterial assemblage associated with mucous secretions of the hydrothermal vent polychaete Paralvinella palmiformis FEMS Microbiol. Ecol. 42 2002 463 476 (Pubitemid 35346600)
46. M.-A. Cambon-Bonavita, G. Raguenes, J. Jean, P. Vincent, and J. Guezennec A novel polymer produced by a bacterium isolated from a deep-sea hydrothermal vent polychaete annelid J. Appl. Microbiol. 93 2002 310 315 (Pubitemid 34989150)
47. C.J. Plante, P.A. Jumars, and J.A. Baross Digestive associations between marine detritivores and bacteria Ann. Rev. Ecol. Syst. 21 1990 93 127 (Pubitemid 120024466)
48. W.W. Lau, P.A. Jumars, and E.V. Armbrust Genetic diversity of attached bacteria in the hindgut of the deposit-feeding shrimp Neotrypaea (formerly Callianassa) californiensis (Decapoda: Thalassinidae) Microbial. Ecol. V43 2002 455 466 (Pubitemid 36941336)
49. J. Harris, L. Seiderer, and M. Lucas Gut microflora of two saltmarsh detritivore thalassinid prawns, Upogebia africana and Callianassa kraussi Microb. Ecol. 21 1991 277 296
50. J.M. Harris Widespread occurrence of extensive epimural rod bacteria in the hindguts of marine Thalassinidae and Brachyura (Crustacea: Decapoda) Mar. Biol. 116 1993 615 629 (Pubitemid 24407457)
51. C. Hoyoux, M. Zbinden, S. Samadi, F. Gaill, and P. Compre Wood-based diet and gut microflora of a galatheid crab associated with Pacific deep-sea wood falls Mar. Biol. 156 2009 2421 2439
52. Y. Wang, U. Stingl, F. Anton-Erxleben, S. Geisler, A. Brune, M. Zimmer, "Candidatus Hepatoplasma crinochetorum", a New, Stalk-Forming Lineage of Mollicutes Colonizing the Midgut Glands of a Terrestrial Isopod, 2004, pp. 6166-72.
53. Y. Wang Symbiotic bacteria in hepatopancreas (midgut glands) of isopods (Crustacea: Isopoda): phylogeny, evolution and distribution 2004 Zoologisches Institut Abteilung Limnologie Christian-Albrechts University of Kiel, Kiel pp. 147
54. E.H. Pinn, L.A. Nickell, A. Rogerson, and R.J.A. Atkinson Comparison of gut morphology and gut microflora of seven species of mud shrimp (Crustacea: Decapoda: Thalassinidea) Mar. Biol. 133 1999 103 114 (Pubitemid 29083758)
55. A. Demiri, A. Meziti, S. Papaspyrou, M. Thessalou-Legaki, and K. Kormas Abdominal setae and midgut bacteria of the mudshrimp Pestarella tyrrhena Cent. Eur. J. Biol. 4 2009 558 566
56. M. Hugler, J.M. Petersen, N. Dubilier, J.F. Imhoff, and S.M. Sievert Pathways of carbon and energy metabolism of the epibiotic community associated with the Deep-Sea Hydrothermal Vent Shrimp Rimicaris exoculata PLoS ONE 6 2011 16018
57. J.A. Breznak, and H.S. Pankratz In situ morphology of the gut microbiota of wood-eating termites Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki Appl. Environ. Microbiol. 33 1977 406 426
58. J.A. Breznak Intestinal Microbiota of Termites and other Xylophagous Insects Ann. Rev. Microbiol. 36 1982 323
59. S. Chaffron, and C. Von Mering Termites in the Woodwork Genome Biol. 8 2007 229
60. C. Bayon Volatile fatty acids and methane production in relation to anaerobic carbohydrate fermentation in Oryctes nasicornis larvae (Coleoptera: Scarabaeidae) J. Insect Physiol. 26 1980 819 828
61. J.E. Dugas, L. Zurek, B.J. Paster, B.A. Keddie, and E.R. Leadbetter Isolation and characterization of a Chryseobacterium; strain from the gut of the American cockroach, Periplaneta americana Arch. Microbiol. 175 2001 259 262 (Pubitemid 32391397)
62. H.-W. Oh, S.-Y. Heo, D. Kim, D.-S. Park, K. Bae, and H.-Y. Park Biochemical Characterization and Sequence Analysis of a Xylanase Produced by an Exo-Symbiotic Bacterium of Gryllotalpa orientalis, Cellulosimicrobium sp. HY-12 Antonie Van Leeuwenhoek 93 2008 437 442
63. S.H.P. Maddrell, and B.O.C. Gardiner The permeability of the cuticular lining of the insect alimentary canal J. Exp. Biol. 85 1980 227 237
64. P. Compre, C. Jeuniaux, and G. Goffinet The integument: morphology and biochemestry Koninklijke Anatomy, taxonomy and biology (crustacean) 2004 Brill Leiden 59 144
65. R. Ley, M. Hamady, C. Lozupone, P. Turnbaugh, R. Ramey, J. Bircher, M. Shlegel, T. Tucker, M. Schrenzel, R. Knight, and J. Gordon Evolution of mammals and their gut microbes Science 320 2008 1647 1651 (Pubitemid 351931256)
66. P. Worthen, C. Gode, and J. Graf Culture-independent characterization of the digestive tract microbiota of the medicinal leech reveals a tripartite symbiosis Appl. Environ. Microbiol. 72 2006 4775 4781 (Pubitemid 44078804)
67. P. Lopez-Garcia, S. Duperron, P. Philippot, J. Foriel, J. Susini, and D. Moreira Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge Environ. Microbiol. 5 2003 961 976 (Pubitemid 37181567)
68. D.J. Harrington Bacterial collagenases and collagen-degrading enzymes and their potential role in human disease Infect. Immun. 64 1996 1885 1891 (Pubitemid 26165642)
69. F. Pradillon, and F. Gaill Adaptation to deep-sea hydrothermal vents: some molecular and developmental aspects J. Mar. Sci. Technol. 15 2007 37 53 (Pubitemid 350247437)
70. S.K. Goffredi, S.B. Johnson, and R.C. Vrijenhoek Genetic diversity and potential function of microbial symbionts associated with newly discovered species of osedax polychaete worms Appl. Environ. Microbiol. 73 2007 2314 2323 (Pubitemid 46649524)