Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four mid-atlantic ridge hydrothermal vent fields

Environmental Microbiology

Volumn 12, Issue 8, 2010, Pages 2204-2218

  Petersen, Jillian M ^a   Ramette, Alban ^a   Lott, Christian ^a,b   Cambon Bonavita, Marie Anne ^c   Zbinden, Magali ^d   Dubilier, Nicole ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b HYDRA Institute for Marine Sciences   (Italy)

^c Centre National de la Recherche Scientifique   (France)

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; MITOCHONDRIAL DNA; RNA 16S;

ANIMAL; ARTICLE; CLASSIFICATION; DECAPODA (CRUSTACEA); DNA SEQUENCE; EPSILONPROTEOBACTERIA; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENETICS; GILL; GROWTH, DEVELOPMENT AND AGING; HYDROTHERMAL VENT; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS;

ANIMALS; DECAPODA (CRUSTACEA); DNA, BACTERIAL; DNA, MITOCHONDRIAL; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GILLS; HYDROTHERMAL VENTS; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); DECAPODA (CRUSTACEA); EPSILONPROTEOBACTERIA; LEUCOTHRIX MUCOR; MUCOR; RIMICARIS EXOCULATA;

EID: 77955249226     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.02129.x     Document Type: Article

References (74)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
2. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S ribosomal RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 1990, 56:1919-1925.
3. Brock TD. The habitat of Leucothrix mucor, a widespread marine microorganism. Limnol Oceanogr 1966, 11:303-307.
4. Bulgheresi S, Schabussova I, Chen T, Mullin NP, Maizels RM, Ott JA. A new C-type lectin similar to the human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Appl Environ Microbiol 2006, 72:2950-2956.
5. Casanova B, Brunet M, Segonzac M. L'impact d'une épibiose bactérienne sur la morphologie fonctionelle de crevettes associées à l'hydrothermalisme médio-atlantique. Cah Biol Mar 1993, 34:573-588.
6. Cavanaugh CM, Robinson JJ. CO2 fixation in chemoautotrophic-invertebrate symbioses: expression of form I and form II RubisCO. Microbial Growth on C1 Compounds 1996, 285-292. Lidstrom ME, Tabita FR., Dordrecht, the Netherlands, Kluwer
7. Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ. Marine chemosynthetic symbioses. The Prokaryotes: An Evolving Electronic Resource for the Microbial Community 2006, 475-507. Dworkin M, Falkow SI, Rosenberg E, Schleifer K-HStackebrandt E., New York, USA, Springer
8. Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N. Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14'N, MAR). Chem Geol 2002, 191:345-359.
9. Chu KH, Li CP, Ho HY. The first internal transcribed spacer (ITS-1) of ribosomal DNA as a molecular marker for phylogenetic and population analyses in Crustacea. Mar Biotechnol 2001, 3:355-361.
10. Corbari L, Zbinden M, Cambon-Bonavita MA, Gaill F, Compere P. Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquat Biol 2007, 1:225-238.
11. Creasey S, Rogers AD, Tyler PA. Genetic comparison of two populations of the deep-sea vent shrimp Rimicaris exoculata (Decapoda: Bresiliidae) from the Mid-Atlantic Ridge. Mar Biol 1996, 125:473-482.
12. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 1999, 22:434-444.
13. DeChaine EG, Bates AE, Shank TM, Cavanaugh CM. Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ Microbiol 2006, 8:1902-1912.
14. Diaz CL, Melchers LS, Hooykaas PJJ, Lugtenberg BJJ, Kijne JW. Root lectin as a determinant of host-plant specificity in the Rhizobium-legume symbiosis. Nature 1989, 338:579-581.
15. Dubilier N, Bergin C, Lott C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 2008, 6:725-739.
16. Duperron S, Bergin C, Zielinski F, Blazejak A, Pernthaler A, McKiness ZP. A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ Microbiol 2006, 8:1441-1447.
17. Folmer O, Black MB, Hoeh WR, Lutz RA, Vrijenhoek RC. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from metazoan invertebrates. Mol Mar Biol Biotechnol 1994, 3:294-299.
18. Galchenko VF, Pimenov NV, Lein AI, Galkin SV, Moskalev LI, Ivanov MV. Autotrophic CO2 assimilation in tissues of prawn Rimicaris exoculata from the Mid-Atlantic Ridge hydrothermal area. Doklady Akademii Nauk SSSR 1989, 308:1478-1481.
19. Gebruk AV, Pimenov NV, Savvichev AS. Feeding specialization of bresiliid shrimps in the TAG site hydrothermal community. Mar Ecol Prog Ser 1993, 98:247-253.
20. Gebruk AV, Southward EC, Kennedy H, Southward AJ. Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Mar Biol Assoc UK 2000, 80:485-499.
21. Gloter A, Zbinden M, Guyot F, Gaill F, Colliex C. TEM-EELS study of natural ferrihydrite from geological-biological interactions in hydrothermal systems. Earth Planet Sci Lett 2004, 222:947-957.
22. Goffredi SK, Waren A, Orphan VJ, Van Dover CL, Vrijenhoek RC. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl Environ Microbiol 2004, 70:3082-3090.
23. Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC. Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ Microbiol 2008, 10:2623-2634.
24. Gourdine JP, Markiv A, Smith-Ravin J. The three-dimensional structure of codakine and related marine C-type lectins. Fish Shellfish Immunol 2007, 23:831-839.
25. Grabovich MY, Muntyan MS, Lebedeva VY, Ustiyan VS, Dubinina GA. Lithoheterotrophic growth and electron transfer chain components of the filamentous gliding bacterium Leucothrix mucor DSM 2157 during oxidation of sulfur compounds. FEMS Microbiol Lett 1999, 178:155-161.
26. Gros O, Liberge M, Heddi A, Khatchadourian C, Felbeck H. Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (Thalassia testudinum environment). Appl Environ Microbiol 2003, 69:6264-6267.
27. Hall T. BioEdit. 1997-2001, http://www.mbio.ncsu.edu/BioEdit/bioedit.html, WWW document]. URL
28. Harmer TL, Rotjan RD, Nussbaumer AD, Bright M, Ng AW, DeChaine EG, Cavanaugh CM. Free-living tube worm endosymbionts found at deep-sea vents. Appl Environ Microbiol 2008, 74:3895-3898.
29. Harrison JS. Phylogeny, biogeography, and speciation in the genus Austinixa and related genera (Crustacea: Brachyura: Pinnotheridae). 2001, PhD Thesis. College Station, TX, USA: Texas A&M University
30. Haselkorn TS, Markow TA, Moran NA. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 2009, 18:1294-1305.
31. Hunter RL, Webb MS, Iliffe TM, Bremer JRA. Phylogeny and historical biogeography of the cave-adapted shrimp genus Typhlatya (Atyidae) in the Caribbean Sea and Western Atlantic. J Biogeogr 2008, 35:65-75.
32. Inagaki F, Takai K, Nealson KH, Horikoshi K. Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 2004, 54:1477-1482.
33. Jannasch HW, Wirsen CO, Molyneaux SJ. Chemosynthetic microbial activity at the 23° and 26°N Mid-Atlantic Ridge vent sites. Ridge Events 1991, 19.
34. Kimura H, Sato M, Sasayama Y, Naganuma T. Molecular characterization and in situ localization of endosymbiotic 16S ribosomal RNA and RuBisCO genes in the pogonophoran tissue. Mar Biotechnol 2003, 5:261-269.
35. Komai T, Segonzac M. Taxonomic review of the hydrothermal vent shrimp genera Rimicaris Williams & Rona and Chorocaris Martin & Hessler (Crustacea: Decapoda: Caridea: Alvinocarididae). J Shellfish Res 2008, 27:21-41.
36. Lee KH, Ruby EG. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 1994, 60:1565-1571.
37. Lösekann T, Robador A, Niemann H, Knittel K, Boetius A, Dubilier N. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic Cold Seep (Haakon Mosby Mud Volcano, Barents Sea). Environ Microbiol 2008, 10:3237-3254.
38. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar. ARB: a software environment for sequence data. Nucleic Acids Res 2004, 32:1363-1371.
39. Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG. A single regulatory gene is sufficient to alter bacterial host range. Nature 2009, 458:215-217.
40. Meng XH, Wang QY, Jang IK, Liu P, Kong J. Genetic differentiation in seven geographic populations of the fleshy shrimp Penaeus (Fenneropenaeus) chinensis based on microsatellite DNA. Aquaculture 2009, 287:46-51.
41. Miethling R, Wieland G, Backhaus H, Tebbe CC. Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb Ecol 2000, 40:43-56.
42. Muyzer G, Teske A, Wirsen CO, Jannash HW. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 1995, 164:165-172.
43. Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2004, 2:632-642.
44. Page TJ, Short JW, Humphrey CL, Hillyer MJ, Hughes JM. Molecular systematics of the Kakaducarididae (Crustacea: Decapoda: Caridea). Mol Phylogenet Evol 2008, 46:1003-1014.
45. Perner M, Kuever J, Seifert R, Pape T, Koschinsky A, Schmidt K. The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15°N on the Mid-Atlantic Ridge. FEMS Microbiol Ecol 2007, 61:97-109.
46. Pimenov NV, Kalyuzhnaya MG, Khmelenina VN, Mityushina LL, Trotsenko YA. Utilization of methane and carbon dioxide by symbiotrophic bacteria in gills of Mytilidae (Bathymodiolus) from the Rainbow and Logachev hydrothermal fields on the Mid-Atlantic Ridge. Microbiol 2002, 71:587-594.
47. Polz MF, Cavanaugh CM. Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proc Natl Acad Sci USA 1995, 92:7232-7236.
48. Polz MF, Robinson JJ, Cavanaugh CM, Van Dover CL. Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnol Oceanogr 1998, 43:1631-1638.
49. Pond D, Dixon D, Sargent J. Wax-ester reserves facilitate dispersal of hydrothermal vent shrimps. Mar Ecol Prog Ser 1997, 146:289-290.
50. Pond DW, Gebruk A, Southward EC, Southward AJ, Fallick AE, Bell MV, Sargent JR. Unusual fatty acid composition of storage lipids in the bresilioid shrimp Rimicaris exoculata couples the photic zone with MAR hydrothermal vent sites. Mar Ecol Prog Ser 2000, 198:171-179.
51. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007, 35:7188-7196.
52. Rieley G, Van Dover CL, Hedrick DB, Eglinton G. Trophic ecology of Rimicaris exoculata: a combined lipid abundance stable isotope approach. Mar Biol 1999, 133:495-499.
53. Robinson JJ, Polz MF, Fiala-Medioni A, Cavanaugh CM. Physiological and immunological evidence for two distinct C1-utilizing pathways in Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), a dual endosymbiotic mussel from the Mid-Atlantic Ridge. Mar Biol 1998, 132:625-633.
54. Ruby EG. Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 2008, 6:752-762.
55. Schmidt K, Koschinsky A, Garbe-Schonberg D, de Carvalho LM, Seifert R. Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15°N on the Mid-Atlantic Ridge: temporal and spatial investigation. Chem Geol 2007, 242:1-21.
56. Schmidt C, Le Bris N, Gaill F. Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J Shellfish Res 2008a, 27:79-90.
57. Schmidt C, Vuillemin R, Le Gall C, Gaill F, Le Bris N. Geochemical energy sources for microbial primary production in the environment of hydrothermal vent shrimps. Mar Chem 2008b, 108:18-31.
58. Segonzac M, Desaintlaurent M, Casanova B. Enigma of the trophic adaptation of the shrimp Alvinocarididae in hydrothermal areas along the Mid-Atlantic Ridge. Cah Biol Mar 1993, 34:535-571.
59. Shank TM, Lutz RA, Vrijenhoek RC. Molecular systematics of shrimp (Decapoda: Bresiliidae) from deep-sea hydrothermal vents, I: enigmatic 'small orange' shrimp from the Mid-Atlantic Ridge are juvenile Rimicaris exoculata. Mol Mar Biol Biotechnol 1998, 7:88-96.
60. Southward AJ, Newman WA. Ectosymbiosis between filamentous sulphur bacteria and a stalked barnacle (Scalpellomorpha, Neolepadinae) from the Lau Back Arc Basin, Tonga. Cah Biol Mar 1998, 39:259-262.
61. Steedman HF. Polyester wax - new ribboning embedding medium for histology. Nature 1957, 179:1345-1345.
62. Suzuki Y, Suzuki M, Tsuchida S, Takai K, Horikoshi K, Southward AJ. Molecular investigations of the stalked barnacle Vulcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand. J Mar Biol Assoc UK 2009, 89:727-733.
63. Teske PR, Froneman PW, Barker NP, McQuaid CD. Phylogeographic structure of the caridean shrimp Palaemon peringueyi in South Africa: further evidence for intraspecific genetic units associated with marine biogeographic provinces. Afr J Mar Sci 2007, 29:253-258.
64. Tyler PA, Young CM. Reproduction and dispersal at vents and cold seeps. J Mar Biol Assoc UK 1999, 79:193-208.
65. Tyler PA, Young CM. Dispersal at hydrothermal vents: a summary of recent progress. Hydrobiologia 2003, 503:9-19.
66. Van Dover CL. The Ecology of Deep-Sea Hydrothermal Vents 2000, Princeton, NJ, USA, Princeton University Press
67. Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA. Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar Biol 1988, 98:209-216.
68. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC. Marine biology - evolution and biogeography of deep-sea vent and seep invertebrates. Science 2002, 295:1253-1257.
69. Vrijenhoek RC. Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Hered 1997, 88:285-293.
70. Williams AB, Rona PA. Two new caridean shrimps (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. J Crustacean Biol 1986, 6:446-462.
71. Wirsen CO, Jannasch HW, Molyneaux SJ. Chemosynthetic microbial sctivity at Mid-Atlantic Ridge hydrothermal vent sites. J Geophys Res 1993, 98:9693-9703.
72. Zbinden M, Cambon-Bonavita MA. Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Ecol 2003, 46:23-30.
73. Zbinden M, Le Bris N, Gaill F, Compere P. Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog Ser 2004, 284:237-251.
74. Zbinden M, Shillito B, Le Bris N, de Montlaur CD, Roussel E, Guyot F. New insigths on the metabolic diversity among the epibiotic microbial communitiy of the hydrothermal shrimp Rimicaris exoculata. J Exp Mar Biol Ecol 2008, 359:131-140.