Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

ISME Journal

Volumn 7, Issue 1, 2013, Pages 96-109

  Ponsard, Julie ^a   Cambon Bonavita, Marie Anne ^b   Zbinden, Magali ^c   Lepoint, Gilles ^a   Joassin, André ^a   Corbari, Laure ^d   Shillito, Bruce ^c   Durand, Lucile ^b   Cueff Gauchard, Valérie ^b   Compère, Philippe ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b Centre National de la Recherche Scientifique   (France)

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

^d MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

autoradiography; chemosynthetic ectosymbiosis; Crustacea; isotopes; Rimicaris exoculata; transtegumental transfer

Indexed keywords

ABSORPTION; CRUSTACEAN; DOMINANCE; FIXATION; HOST-SYMBIONT INTERACTION; HYDROTHERMAL VENT; INORGANIC CARBON; METABOLISM; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; NUTRITION; ORGANIC COMPOUND; RADIOGRAPHY;

ANIMAL; ARTICLE; CARBON CYCLE; CHEMOAUTOTROPHY; DECAPODA (CRUSTACEA); EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GILL; HYDROTHERMAL VENT; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; CARBON CYCLE; CHEMOAUTOTROPHIC GROWTH; DECAPODA (CRUSTACEA); EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GILLS; HYDROTHERMAL VENTS; SYMBIOSIS;

ATLANTIC OCEAN; MID-ATLANTIC RIDGE;

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

EID: 84871386059     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.87     Document Type: Article

References (80)

1. Ahearn H, Ahearn G, Gomme J. (2000). Integumentary L-histidine transport in a euryhaline polychaete worm: regulatory roles of calcium and cadmium in the transport event. J Exp Biol 203: 2877-2885.
2. Anderson JW, Stephens GC. (1969). Uptake of organic material by aquatic invertebrates. VI. Role of epiflora in apparent uptake of glycine by marine crustaceans. Mar Biol 4: 243-249.
3. Bresciani J, Høeg JT. (2001). Comparative ultrastructure of the root system in Rhizocephalan barnacles (Crustacea: Cirripedia: Rhizocephala). J Morphol 249: 9-42.
4. Campbell BJ, Engel AS, Porter ML, Takai K. (2006). The versatile e-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468.
5. CAREX Identification of model organisms in extreme environments. CAREX-Workshop Report; 5 November 2010; Sasbachwalden (Black Forest) Germany http://www.carex-eu.org/.
6. Casanova B, Brunet M, Ségonzac M. (1993). L'impact d'une épibiose bactérienne sur la morphologie fonctionnelle de crevettes associées à l'hydrothermalisme Médio-Atlantique. Cah Biol Mar 34: 573-588.
7. Cavanaugh C, McKiness Z, Newton I, Stewart F. (2006). Marine Chemosynthetic Symbioses. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds). The Prokaryotes. Springer Science Business Media, Inc.: Singapore, pp 475-507.
8. Charlou J-L, Donval J-P, Fouquet Y, Jean-Baptiste P, Holm N. (2002). Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (361140N, MAR). Chem Geol 191: 345-359.
9. Childress JJ, Fisher CR, Favuzzi JA, Sanders NK. (1991). Sulfide and carbon dioxide uptake by the hydrothermal vent clam, Calyptogena magnifica, and its chemoautotrophic symbionts. Physiol Zool 64: 1444-1470.
10. Chipps SR. (1998). Temperature-dependent consumption and gut-residence time in the opossum shrimp Mysis relicta. J Plankton Res 20: 2401-2411.
11. Colaço A, Desbruyères D, Guezennec J. (2007). Polar lipid fatty acids as indicators of trophic associations in a deep-sea vent system community. Mar Ecol 28: 15-24.
12. Compère P, Jeuniaux C, Goffinet G. (2004). The integument: morphology and biochemistry. In: Forest J, Van Vaupel Klein JC (eds). Treatise on Zoology, 1. Anatomy, Taxonomy and Biology, The Crustacea. vol. 1: Brill, Leiden, pp 59-144.
13. Corbari L, Cambon-Bonavita M-A, Long GJ, Grandjean F, Zbinden M, Gaill F et al. (2008a). Iron oxide deposits associated with the ectosymbiotic bacteria in the hydrothermal vent shrimp Rimicaris exoculata. Biogeosciences 5: 1295-1310.
14. Corbari L, Zbinden M, Cambon-Bonavita M-A, Gaill F, Compère P. (2008b). Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle. Aquat Biol 1: 225-238.
15. Dattagupta S, Schaperdoth I, Montanari A, Mariani S, Kita N, Valley JW et al. (2009). A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. ISME J 3: 935-943.
16. De Eguileor M, Leonardi MG, Grimaldi A, Tettamanti G, Fiandra L, Giordana B et al. (2000). Integumental amino acid uptake in a carnivorous predator mollusc (Sepia officinalis, Cephalopoda). Tissue Cell 32: 389-399.
17. Douville E, Charlou J-L, Oelkers EH, Bienvenu P, Jove Colon CF, Donval J-P et al. (2002). The rainbow vent fluids (361140N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in Mid-Atlantic Ridge hydrothermal fluids. Chem Geol 184: 37-48.
18. Dubilier N, Bergin C, Lott C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6: 725-740.
19. Dubilier N, Mulders C, Ferdelman T, de Beer D, Pernthaler A, Klein M et al. (2001). Endosymbiotic sulphatereducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411: 298-302.
20. Durand L, Zbinden M, Cueff-Gauchard V, Duperron S, Roussel EG, Shillito B et al. (2010). Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol Ecol 71: 291-303.
21. Felbeck H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila jones (Vestimentifera). Science 213: 336-338.
22. Fisher CR, Childress JJ, Minnich E. (1989). Autotrophic carbon fixation by the chemoautotrophic symbionts of Riftia pachyptila. Biol Bull 177: 372-385.
23. Fleming MW, Fetterer RH. (1984). Ascaris suum: continuous perfusion of the pseudocoelom and nutrient absorption. Exp Parasitol 57: 142-148.
24. Gebruk AV, Pimenov NV, Savvichev AS. (1993). Feeding specialization of bresiliid shrimps in the TAG site hydrothermal community. Mar Ecol Prog Ser 98: 247-253.
25. Gebruk AV, Southward EC, Kennedy H, Southward AJ. (2000). Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Mar Biol Assoc UK 80: 485-499.
26. Gillan DC, Dubilier N. (2004). Novel epibiotic Thiothrix bacterium on a marine Amphipod. Appl Environ Microbiol 70: 3772-3775.
27. Gillan DC, Ribesse J, De Ridder C. (2004). The ironencrusted microbial community of Urothoe poseidonis (Crustacea, Amphipoda). J Sea Res 52: 21-32.
28. Goffredi SK. (2010). Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates. Environ Microbiol Rep 2: 479-488.
29. Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC. (2008). Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ Microbiol 10: 2623-2634.
30. Gordon R, Burford IR. (1984). Transport of palmitic acid across the tegument of the entomophilic nematode Romanomermis culicivorax. J Nematol 16: 14-21.
31. Guri M, Durand L, Cueff-Gauchard V, Zbinden M, Crassous P, Shillito B et al. (2012). Acquisition of epibiotic bacteria along the life cycle of the hydrothermal shrimp Rimicaris exoculata. ISME J 6: 597-609.
32. Hoyt M, Fleeger JW, Siebeling R, Feller RJ. (2000). Serological estimation of prey-protein gut-residence time and quantification of meal size for grass shrimp consuming meiofaunal copepods. J Exp Mar Biol Ecol 248: 105-119.
33. Hügler M, Gärtner A, Imhoff JF. (2010). Functional genes as markers for sulfur cycling and CO2 fixation in microbial communities of hydrothermal vents of the Logatchev field. FEMS Microbiol Ecol 73: 526-537.
34. Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM. (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.
35. Kannupandi T. (1976). Cuticular adaptations in two parasitic copepods in relation to their modes of life. J Exp Mar Biol Ecol 22: 235-248.
36. Kleiner M,Wentrup C, Lott C, Teeling H,Wetzel S, Young J et al. (2012). Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proc Natl Acad Sci 109: E1173-E1182.
37. Larkin JM, Strohl WR. (1983). Beggiatoa, Thiothrix, and Thioploca. Annu Rev Microbiol 37: 341-367.
38. Lepoint G, Gobert S, Dauby P, Bouquegneau J-M. (2004). Contributions of benthic and planktonic primary producers to nitrate and ammonium uptake fluxes in a nutrient-poor shallow coastal area (Corsica, NW Mediterranean). J Exp Mar Biol Ecol 302: 107-122.
39. Macpherson E, Jones WJ, Segonzac M. (2005). A new squat lobster family of Galatheoidea (Crustacea, Decapoda, Anomura) from the hydrothermal vents of the Pacific-Antarctic Ridge. Zoosystema 27: 709-723.
40. Martinez A-S, Charmantier G, Compère P, Charmantier-Daures M. (2005). Branchial chamber tissues in two caridean shrimps: the epibenthic Palaemon adspersus and the deep-sea hydrothermal Rimicaris exoculata. Tissue Cell 37: 153-165.
41. Masood K. (1984). Transcuticular absorption of amino acids by Ascaridia galli. Indian J Parasitol 7: 185-188.
42. Miyake H, Kitada M, Tsuchida S, Okuyama Y, Nakamura K-i. (2007). Ecological aspects of hydrothermal vent animals in captivity at atmospheric pressure. Mar Ecol 28: 86-92.
43. Nelson DC, Hagen KD, Edwards DB. (1995). The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium. Mar Biol 121: 487-495.
44. Peppler JE, Ahearn GA. (2003). Effect of heavy metals on the uptake of [3H]-L-histidine by the polychaete Nereis succinea. Comp Biochem Physiol C Toxicol Pharmacol 136: 181-189.
45. Petersen JM, Ramette A, Lott C, Cambon-Bonavita M-A, Zbinden M, Dubilier N. (2009). 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.
46. Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R et al. (2011). Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476: 176-180.
47. Polz MF, Cavanaugh CM. (1995). Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proc Natl Acad Sci USA 92: 7232-7236.
48. Polz MF, Cavanaugh CM. (1996). The ecology of ectosymbiosis at a Mid-Atlantic Rigde hydrothermal vent site. Biosyst Ecol Ser 11: 337-352.
49. Polz MF, Robinson JJ, Cavanaugh CM, Van Dover CL. (1998). Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnol Oceanogr 43: 1631-1638.
50. Pond DW, Bell MV, Dixon DR, Fallick AE, Sargent J.R. (1997a). Occurrence of 16:2(n-4) and 18:2(n-4) fatty acids in the lipids of the hydrothermal vent shrimp Rimicaris exoculata: nutritional and trophic implications. Marine Ecology Progress Series 156: 167-174.
51. Pond DW, Gebruk A, Southward EC, Southward AJ, Fallick AE, Bell MV et al. (2000). 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 198: 171-179.
52. Pond DW, Segonzac M, Bell MV, Dixon DR, Fallick AE, Sargent JR. (1997b). Lipid and lipid carbon stable isotope composition of the hydrothermal vent shrimp Mirocaris fortunata: evidence for nutritional dependence on photosynthetically fixed carbon. Mar Ecol Prog Ser 157: 221-231.
53. Poquet M, Ribes E, Bozzo MG, Durfort M. (1994). Ultrastructure and cytochemistry of the integument of Modiolicola gracilis, parasitic copepod in mussel gills (Mytilus galloprovincialis and Mytilus edulis). J Morphol 221: 87-99.
54. Preston RL. (1993). Transport of amino acids by marine invertebrates. J Exp Zool 265: 410-421.
55. Ravaux J, Gaill F, Le Bris N, Sarradin P-M, Jollivet D, Shillito B. (2003). Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J Exp Biol 206: 2345-2354.
56. Richards KS, Arme C. (1982). Integumentary uptake of dissolved organic materials by earthworms. Pedobiologia 23: 358-366.
57. Rieley G, Van Dover CL, Hedrick DB, Eglinton G. (1999). Trophic ecology of Rimicaris exoculata: a combined lipid abundance/stable isotope approach. Mar Biol 133: 495-499.
58. Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T et al. (2008). Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10: 727-737.
59. Rouwenhorst RJ, Frank Jzn J, Scheffers WA, Van Dijken JP. (1991). Determination of protein concentration by total organic carbon analysis. J Biochem Biophys Methods 22: 119-128.
60. Schmidt C, Corbari L, Gaill F, 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.
61. Schmidt C, Vuillemin R, Le Gall C, Gaill F, Le Bris N. (2008). Geochemical energy sources for microbial primary production in the environment of hydrothermal vent shrimps. Mar Chem 108: 18-31.
62. Schulz HN, Jørgensen BB. (2001). Big Bacteria. Annu Rev Microbiol 55: 105-137.
63. Scott KM, Cavanaugh CM. (2007). CO2 uptake and fixation by endosymbiotic chemoautotrophs from the Bivalve Solemya velum. Appl Environ Microbiol 73: 1174-1179.
64. Segonzac M. (1992). The hydrothermal vent communities of Snake Pit area (Mid-Atlantic Ridge; 231N, 3480 m): megafaunal composition and microdistribution. Mar Biol 314: 593-600.
65. Segonzac M, De Saint Laurent M, Casanova B. (1993). L'énigme du comportement trophique des crevettes Alvinocarididae des sites hydrothermaux de la dorsale médio-atlantique. Cah Biol Mar 34: 535-571.
66. Shillito B, Jollivet D, Sarradin P-M, Rodier P, Lallier F, Desbruyères D et al. (2001). Temperature resistance of Hesiolyra bergi, a polychaetous annelid living on deep-sea vent smoker walls. Mar Ecol Prog Ser 216: 141-149.
67. Stams AJM, Plugge CM. (2009). Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7: 568-577.
68. Stephens GC. (1988). Epidermal amino acid transport in marine invertebrates. Biochim Biophys Acta 947: 113-138.
69. Stewart FJ, Cavanaugh CM. (2006). Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)-model systems for studies of symbiont-host adaptation. Antonie Van Leeuwenhoek 90: 343-360.
70. Thurber AR, Jones WJ, Schnabel K. (2011). Dancing for food in the Deep Sea: bacterial farming by a new species of yeti crab. PLoS ONE 6: e26243.
71. Ullberg S, Larsson B, Tjälve H. (1982). Autoradiography. In: Glenn HJ (ed). Biologic Applications of Radiotracers. CRC Press: Boca Raton, Florida pp 55-108.
72. Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA. (1988). Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar Biol 98: 209-216.
73. Williams AB, Rona PA. (1986). Two new caridean shrimps (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. J Crust Biol 6: 446-462.
74. Wirsen CO, Jannasch HW, Molyneaux SJ. (1993). Chemosynthetic microbial activity at Mid-Atlantic Ridge hydrothermal vent sites. J Geophys Res 98: 9693-9703.
75. Wright SH. (1988). Amino acid transport in the gill epithelium of a marine bivalve. Comp Biochem Physiol A Physiol 90: 635-641.
76. Wright SH, Pajor AM. (1989). Mechanisms of integumental amino acid transport in marine bivalves. Am J Physiol 257: R473-R483.
77. Wright SH, Secomb TW. (1986). Epithelial amino acid transport in marine mussels: role in net exchange of taurine between gills and sea water. J Exp Biol 121: 251-270.
78. Zbinden M, Cambon-Bonavita M-A. (2003). Occurrence of Deferribacterales and Entomoplasmatales in the deepsea Alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Ecol 46: 23-30.
79. Zbinden M, Le Bris N, Gaill F, 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 Prog Ser 284: 237-251.
80. Zbinden M, Shillito B, Le Bris N, De Villardi de Montlaur C, Roussel E, Guyot F et al. (2008). New insights on the metabolic diversity among the epibiotic microbial communitiy of the hydrothermal shrimp Rimicaris exoculata. J Exp Mar Biol Ecol 359: 131-140.