Symbiosis of Thioautotrophic Bacteria with Riftia pachyptila

  • Frank J. Stewart
  • Colleen M. Cavanaugh
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 41)


Bacterial Symbiont Bacterial Endosymbiont Symbiont Population Symbiont Cell Symbiont Transmission 
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  1. Alt JC (1995) Subseafloor processes in mid-ocean ridge hydrothermal systems. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological Interactions. Geophysical monograph 91. Am Geophys Union, Washington, DC, pp 85–114Google Scholar
  2. Arndt C, Gaill F, Felbeck H (2001) Anaerobic sulfur metabolism in thiotrophic symbioses. J Exp Biol 204:741–750PubMedGoogle Scholar
  3. Arp AJ, Childress JJ, Fisher CR (1985) Blood gas transport in Riftia pachyptila. Bull Biol Soc Wash 6:289–300Google Scholar
  4. Arp AJ, Childress JJ, Vetter RD (1987) The sulphide-binding protein in the blood of the vestimentiferan tube-worm, Riftia Pachyptila, is the extracellular haemoglobin. J Exp Biol 128:139–158Google Scholar
  5. Bailly X, Jollivet D, Vanin S, Deutsch J, Zal F, Lallier F, Toulmond A (2002) Evolution of the sulfide-binding function within the globin multigenic family of the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Mol Biol Evol 19:1421–1433PubMedGoogle Scholar
  6. Bailly X, Leroy R, Carney S, Collin O, Zal F, Toulmond A, Jollivet D (2003) The loss of the hemoglobin H2S-binding function in annelids from sulfide-free habitats reveals molecular adaptation driven by Darwinian positive selection. Proc Nat Acad Sci USA 100:5885–5890CrossRefPubMedGoogle Scholar
  7. Beynon JD, MacRae IJ, Huston SL, Nelson DC, Segel IH, Fisher AJ (2001) Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. Biochemistry 40:14509–14517CrossRefPubMedGoogle Scholar
  8. Boetius A, Felbeck H (1995) Digestive enzymes in marine-invertebrates from hydrothermal vents and other reducing environments. Mar Biol 122:105–113CrossRefGoogle Scholar
  9. Bosch C, Grassé PP (1984a) Cycle partiel des bactéries chimioautotrophes symbiotiques et eurs rapports avec les bactériocytes chez Riftia pachyptila Jones (Pogonophore Vestimentifère) I. Le trophosome et les bactériocytes. CR Acad Sci III Vie 299:371–376Google Scholar
  10. Bosch C, Grassé PP (1984b) Cycle partiel des bactéries chimioautotrophes symbiotiques et eurs rapports avec les bactériocytes chez Riftia pachyptila Jones (Pogonophore Vestimentifère) II. L’évolution des bactéries symbotiques et des bactériocytes. CR Acad Sci III Vie 299:413–419Google Scholar
  11. Bright M, Sorgo A (2003) Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae). Invert Biol 122:347–368CrossRefGoogle Scholar
  12. Bright M, Keckeis H, Fisher CR (2000) An autoradiographic examination of carbon fixation, transfer and utilization in the Riftia pachyptila symbiosis. Mar Biol 136:621–632CrossRefGoogle Scholar
  13. Cary SC, Warren W, Anderson E, Giovannoni SJ (1993) Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont-specific polymerase chain reaction amplification and in situ hybridization techniques. Mol Mar Biol Biotech 2:51–62Google Scholar
  14. Cavanaugh CM (1983) Symbiotic chemoautotrophic bacteria in marine invertebrates from sulfide-rich habitats. Nature 302:58–61CrossRefGoogle Scholar
  15. Cavanaugh CM (1985) Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Bull Biol Soc Wash 6:373–388Google Scholar
  16. Cavanaugh CM (1994) Microbial symbiosis: patterns of diversity in the marine environment. Am Zool 34:79–89Google Scholar
  17. Cavanaugh CM, Robinson JJ (1996) CO2 fixation in chemoautotroph-invertebrate symbioses: expression of Form I and Form II RubisCO. In: Lidstrom ME, Tabita FR (eds) Microbial growth on C1 compounds. Kluwer Academic Publ Dordrecht, pp 285–292Google Scholar
  18. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342PubMedGoogle Scholar
  19. Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ (2005) Marine chemosynthetic symbioses. In: Dworkin M, Falkow S, Rosenberg E, et al (eds) The Prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, Berlin Heidelberg New York (in press)Google Scholar
  20. Chen XA, Li S, Aksoy S (1999) Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48:49–58CrossRefPubMedGoogle Scholar
  21. Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry, and autotrophic processes. Oceanogr Mar Biol 30:337–441Google Scholar
  22. Childress JJ, Fisher CR, Favuzzi JA, Kochevar RE, Sanders NK, Alayse AM (1991) Sulfide-driven autotrophic balance in the bacterial symbiont-containing hydrothermal vent tubeworm, Riftia pachyptila Jones. Biol Bull 180:135–153Google Scholar
  23. Childress JJ, Lee RW, Sanders NK, Felbeck H, Oros DR, Toulmond A, Desbruyeres D, Kennicutt MC, Brooks J (1993) Inorganic carbon uptake in hydrothermal vent tubeworms facilitated by high environmental pCO2. Nature 362:147–169CrossRefGoogle Scholar
  24. Chua KL, Chan YY, Gan YH (2003) Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71:1622–1629CrossRefPubMedGoogle Scholar
  25. Corliss JB, Dymond J, Gordon LI, Edmond JM, Herzen RPV, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, van Andel TH (1979) Submarine thermal springs on the Galapagos Rift. Science 203:1073–1083PubMedGoogle Scholar
  26. Dale C, Wang B, Moran N, Ochman H (2003) Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20:1188–1194CrossRefPubMedGoogle Scholar
  27. De Cian MC, Andersen AC, Bailly X, Lallier FH (2003a) Expression and localization of carbonic anhydrase and ATPases in the symbiotic tubeworm Riftia pachyptila. J Exp Biol 206:399–409CrossRefPubMedGoogle Scholar
  28. De Cian MC, Bailly X, Morales J, Strub JM, Van Dorsselaer A, Lallier FH (2003b) Characterization of carbonic anhydrases from Riftia pachyptila, a symbiotic invertebrate from deep-sea hydrothermal vents. Proteins 51:327–339CrossRefPubMedGoogle Scholar
  29. Degnan PH, Lazarus AB, Brock CD, Wernegreen JJ (2004) Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus blochmannia. Syst Biol 53:95–110CrossRefPubMedGoogle Scholar
  30. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34:1733–1743CrossRefGoogle Scholar
  31. Di Meo CA, Wilbur AE, Holben WE, Feldman RA, Vrijenhoek RC, Cary SC (2000) Genetic variation among endosymbionts of widely distributed vestimentiferan tubeworms. Appl Environ Microbiol 66:651–658CrossRefPubMedGoogle Scholar
  32. Distel DL, Lane DJ, Olsen GJ, Giovannoni SJ, Pace B, Pace NR, Stahl DA, Felbeck H (1988) Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J Bacteriol 170:2506–2510PubMedGoogle Scholar
  33. Dons L, Eriksson E, Jin YX, Rottenberg ME, Kristensson K, Larsen CN, Bresciani J, Olsen JE (2004) Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72:3237–3244CrossRefPubMedGoogle Scholar
  34. Elderfield H, Schultz A (1996) Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Annu Rev Earth Plant Sci 24:191–224CrossRefGoogle Scholar
  35. Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213:336–338PubMedGoogle Scholar
  36. Felbeck H (1985) CO2 fixation in the hydrothermal vent tube worm Riftia pachyptila (Jones). Physiol Zool 58:272–281Google Scholar
  37. Felbeck H, Jarchow J (1998) Carbon release from purified chemoautotrophic bacterial symbionts of the hydrothermal vent tubeworm Riftia pachyptila. Physiol Zool 71:294–302PubMedGoogle Scholar
  38. Felbeck H, Arndt C, Hentschel U, Childress JJ (2004) Experimental application of vascular and coelomic catheterization to identify vascular transport mechanisms for inorganic carbon in the vent tubeworm, Riftia pachyptila. Deep Sea Res 51:401–411CrossRefGoogle Scholar
  39. Feldman R, Black M, Cary C, Lutz R, Vrijenhoek R (1997) Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mol Mar Biol Biotech 6:268–277Google Scholar
  40. Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436Google Scholar
  41. Fisher CR (1995) Toward an appreciation of hydrothermal vent animals: their environment, physiological ecology, and tissue stable isotope values. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological Interactions. Geophysical monograph 91. Am Geophys Union, Washington, DC, pp 297–316Google Scholar
  42. Fisher CR (1996) Ecophysiology of primary production at deep-sea vents and seeps. In: Uiblein R, Ott J, Stachowtish M (eds) Deep-sea and extreme shallow-water habitats: affinities and adaptations. Biosystematics and ecology series, vol 11. Austrian Academy of Sciences, Vienna, pp 311–334Google Scholar
  43. Fisher, CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, Macko SA, Newton A, Powell MA, Somero GN, Soto T (1988) Physiology, morphology, and biochemical composition of Riftia pachyptila at Rose Garden in 1985. Deep Sea Res 35:1745–1758CrossRefGoogle Scholar
  44. Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW, Royer JR. WE (2005) Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Nat Acad Sci USA 102:2713–2718CrossRefPubMedGoogle Scholar
  45. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882CrossRefPubMedGoogle Scholar
  46. Gardiner SL, Jones ML (1993) Vestimentifera. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates, vol 12. Onychophora, Chilopoda, and lesser Protostomata. Wiley-Liss, New York, pp 371–460Google Scholar
  47. Gavin R, Merino S, Altarriba M, Canals R, Shaw JG, Tomas JM (2003) Lateral flagella are required for increased cell adherence, invasion and biofilm formation by Aeromonas spp. FEMS Microbiol Lett 224:77–83CrossRefPubMedGoogle Scholar
  48. Gebruk AV, Krylova EM, Lein AY, Vinogradov GM, Anderson E, Pimenov NV, Cherkashev GA, Crane K (2003) Methane seep community of the Hakon Mosby mud volcano (the Norwegian Sea): composition and trophic aspects. Sarsia 88:394–403CrossRefGoogle Scholar
  49. Girguis PR, Lee RW, Desaulniers N, Childress JJ, Pospesel M, Felbeck H, Zal F (2000) Fate of nitrate acquired by the tubeworm Riftia pachyptila. Appl Environ Microbiol 66:2783–2790CrossRefPubMedGoogle Scholar
  50. Girguis PR, Childress JJ, Freytag JK, Klose K, Stuber R (2002) Effects of metabolite uptake on proton-equivalent elimination by two species of deep-sea vestimentiferan tubeworm, Riftia pachyptila and Lamellibrachia cf luymesi: proton elimination is a necessary adaptation to sulfide-oxidizing chemoautotrophic symbionts. J Exp Biol 205:3055–3066PubMedGoogle Scholar
  51. Goffredi SK, Childress JJ (2001) Activity and inhibitor sensitivity of ATPases in the hydrothermal vent tubeworm Riftia pachyptila: a comparative approach. Mar Biol 138:259–265CrossRefGoogle Scholar
  52. Goffredi SK, Childress JJ, Desaulniers NT, Lallier FH (1997a) Sulfide acquisition by the hydrothermal vent tubeworm Riftia pachyptila appears to be via uptake of HS, rather than H2S. J Exp Biol 200:2069–2616Google Scholar
  53. Goffredi SK, Childress JJ, Desaulniers NT, Lee RW, Lallier FH, Hammond D (1997b) Inorganic carbon acquisition by the hydrothermal vent tubeworm Riftia pachyptila depends upon high external pCO2 and upon proton-equivalent ion transport by the worm. J Exp Biol 200:883–896PubMedGoogle Scholar
  54. Goffredi SK, Childress JJ, Lallier FH, Desaulniers NT (1999) The ionic composition of the hydrothermal vent tube worm Riftia pachyptila: evidence for the elimination of SO4 2− and H+ and for a Cl/HCO3− shift. Physiol Biochem Zool 72:296–306CrossRefPubMedGoogle Scholar
  55. Grassle JF (1985) Hydrothermal vent animals — distribution and biology. Science 229:713–717PubMedGoogle Scholar
  56. Gros O, De Wulf-Durand P, Frenkiel L, Moueza M (1998) Putative environmental transmission of sulfur-oxidizing bacterial symbionts in tropical lucinid bivalves inhabiting various environments. FEMS Microbiol Lett 160:257–262Google Scholar
  57. Gros O, Liberge M, Heddi A, Khatchadourian C, Felbeck H (2003) Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (Thalassia testudinum environment). Appl Environ Microbiol 69:6264–6267CrossRefPubMedGoogle Scholar
  58. Guy RD, Fogel ML, Berry JA (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101:37–47PubMedGoogle Scholar
  59. Hand SC (1987) Trophosome ultrastructure and the characterization of isolated bacteriocytes from invertebrate-sulfur bacteria symbioses. Biol Bull 173:260–276Google Scholar
  60. Harmer T, Nussbaumer A, Bright M, Cavanaugh CM (2005) Stalking the wild symbiont: free-living counterparts to tubeworm symbionts at deep-sea hydrothermal vents (in preparation)Google Scholar
  61. Hentschel U, Felbeck H (1993) Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila. Nature 366:338–340CrossRefGoogle Scholar
  62. Hughes DS, Felbeck H, Stein JL (1997) A histidine protein kinase homolog from the endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila. Appl Environ Microbiol 63:3494–3498PubMedGoogle Scholar
  63. Johnson KS, Childress JJ, Beehler CL (1988a) Short-term temperature variability in the Rose Garden hydrothermal vent field — an unstable deep-sea environment. Deep Sea Res 35:1711–1721CrossRefGoogle Scholar
  64. Johnson KS, Childress JJ, Hessler RR, Sakamoto-Arnold CM, Beehler CL (1988b) Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep Sea Res 35:1723–1744CrossRefGoogle Scholar
  65. Johnson KS, Childress JJ, Beehler CL, Sakamoto CM (1994) Biogeochemistry of hydrothermal vent mussel communities — the deep sea analog to the intertidal zone. Deep Sea Res 41:993–1011CrossRefGoogle Scholar
  66. Jones ML (1981) Riftia pachyptila Jones: observations on the vestimentiferan worm from the Galapagos Rift. Science 213:333–336PubMedGoogle Scholar
  67. Jones ML, Gardiner SL (1988) Evidence for a transient digestive tract in Vestimentifera. Proc Biol Soc Wash 101:423–433Google Scholar
  68. Kelly DP (1982) Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. In: Postgate JR, Kelly DP (eds) Sulphur bacteria. R Soc Lond, pp 69–98Google Scholar
  69. Kirov SM (2003) Bacteria that express lateral flagella enable dissection of the multifunctional roles of flagella in pathogenesis. FEMS Microbiol Lett 224:151–159CrossRefPubMedGoogle Scholar
  70. Kochevar RE, Childress JJ (1996) Carbonic anhydrase in deep-sea chemoautotrophic symbioses. Mar Biol 125:375–383CrossRefGoogle Scholar
  71. Laue BE, Nelson DC (1994) Characterization of the gene encoding the autotrophic ATP sulfurylase from the bacterial endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila. J Bacteriol 176:3723–3729PubMedGoogle Scholar
  72. Laue BE, Nelson DC (1997) Sulfur-oxidizing symbionts have not co-evolved with their hydrothermal vent tubeworm hosts: an RFLP analysis. Mol Mar Biol Biotech 6:180–188Google Scholar
  73. Lee RW, Childress JJ (1994) Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl Environ Microbiol 60:1852–1858PubMedGoogle Scholar
  74. Lee RW, Robinson JJ, Cavanaugh CM (1999) Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria-marine invertebrate symbioses: expression of host and symbiont glutamine synthetase. J Exp Biol 202:289–300PubMedGoogle Scholar
  75. Lonsdale P (1977) Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep Sea Res 24:857–863CrossRefGoogle Scholar
  76. Lutz RA, Shank TM, Fornari DJ, Haymon RM, Lilley MD, von Damm KL, Desbruyeres D (1994) Rapid growth at deep-sea vents. Nature 371:663–664CrossRefGoogle Scholar
  77. McKiness ZP (2004) Evolution of endosymbioses in deep-sea bathymodioline mussels (Mollusca:Bivalvia). PhD Thesis, Harvard UniversityGoogle Scholar
  78. McMullin ER, Hourdez S, Schaeffer SW, Fisher CR (2003) Phylogeny and biogeography of deep-sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34:1–41Google Scholar
  79. Millero FJ, Plese T, Fernandez M (1987) The dissociation of hydrogen-sulfide in seawater. Limnol Oceanogr 33:269–274CrossRefGoogle Scholar
  80. Millikan DS, Felbeck H, Stein JL (1999) Identification and characterization of a flagellin gene from the endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila. Appl Environ Microbiol 65:3129–3133PubMedGoogle Scholar
  81. Minic Z, Herve G (2003) Arginine metabolism in the deep sea tube worm Riftia pachyptila and its bacterial endosymbiont. J Biol Chem 278(42):40527–40533CrossRefPubMedGoogle Scholar
  82. Minic Z, Herve G (2004) Biochemical and enzymological aspects of the symbiosis between the deep-sea tubeworm Riftia pachyptila and its bacterial endosymbiont. Eur J Biochem 271:3093–3102CrossRefPubMedGoogle Scholar
  83. Minic Z, Simon V, Penverne B, Gaill F, Herve G (2001) Contribution of the bacterial endosymbiont to the biosynthesis of pyrimidine nucleotides in the deep-sea tubeworm Riftia pachyptila. J Biol Chem 276:23777–23784CrossRefPubMedGoogle Scholar
  84. Mira A, Moran NA (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microbial Ecol 44:137–143CrossRefGoogle Scholar
  85. Moran NA (1996) Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93:2873–2878CrossRefPubMedGoogle Scholar
  86. Moran N, Baumann P (1994) Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol Evol 9:15–20CrossRefGoogle Scholar
  87. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9Google Scholar
  88. Nelson DC, Fisher CR (1995) Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. In: Karl DM (ed) Microbiology of deep-sea hydrothermal vents. CRC Press, Boca Raton, pp 125–167Google Scholar
  89. Nelson K, Fisher CR (2000) Absence of cospeciation in deep-sea vestimentiferan tubeworms and their bacterial endosymbionts. Symbiosis 28:1–15Google Scholar
  90. Nelson DC, Hagen KD (1995) Physiology and biochemistry of symbiotic and free-living chemoautotrophic bacteria. Am Zool 35:91–101Google Scholar
  91. Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98CrossRefPubMedGoogle Scholar
  92. Peck HD Jr, LeGall J (1982) Biochemistry of dissimilatory sulphate reduction. In: Postgate JR, Kelly DP (eds) Sulphur bacteria. R Soc Lond, pp 13–36Google Scholar
  93. Peek AS, Vrijenhoek RC, Gaut BS (1998) Accelerated evolutionary rate in sulfuroxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol 15:1514–1523PubMedGoogle Scholar
  94. Pernthaler A, Amann R (2004) Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl Environ Microbiol 70:5426–5433CrossRefPubMedGoogle Scholar
  95. Pimenov NV, Savvichev AS, Rusanov II, Lein AY, Ivanov MV (2000) Microbiological processes of the carbon and sulfur cycles at cold methane seeps of the North Atlantic. Microbiology 69:709–720CrossRefGoogle Scholar
  96. Polz MF, Ott JA, Bright M, Cavanaugh CM (2000) When bacteria hitch a ride. ASM News 66:531–539Google Scholar
  97. Powell MA, Somero GN (1986) Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biol Bull 171:274–290Google Scholar
  98. Rau GH (1981) Hydrothermal vent clam and tube worm 13C/12C: further evidence of non-photosynthetic food sources. Science 213:338–340PubMedGoogle Scholar
  99. Renosto F, Martin RL, Borrell JL, Nelson DC, Segel IH (1991) ATP sulfurylase from trophosome tissue of Riftia pachyptila (hydrothermal vent tube worm). Arch Biochem Biophys 290:66–78CrossRefPubMedGoogle Scholar
  100. Robinson JJ, Cavanaugh CM (1995) expression of from I and form II Rubisco in chemoautotrophic symbioses: implications for the interpretation of stable isotope values. Limnol Oceanogr 40:1496–1502CrossRefGoogle Scholar
  101. Robinson J, Stein JL, Cavanaugh CM (1998) Cloning and sequencing of a form II ribulose-1,5-bisphosphate carboxylase/oxygenase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. J Bacteriol 180:1596–1599PubMedGoogle Scholar
  102. Robinson J, Scott KM, Swanson ST, O’Leary MH, Horken K, Tabita FR, Cavanaugh CM (2003) Kinetic isotope effect and characterization of form II RubisCO from the chemoautotrophic endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila. Limnol Oceanogr 48:48–54CrossRefGoogle Scholar
  103. Roeske CA, O’Leary MH (1984) Carbon isotope effects on the enzyme-catalyzed carboxylation of ribulose bisphosphate. Biochemistry 23:6275–6284CrossRefGoogle Scholar
  104. Roeske CA, O’Leary MH (1985) Carbon isotope effect on carboxylation of ribulose bisphosphate catalyzed by ribulosebisphosphate carboxylase from Rhodospirillum rubrum. Biochemistry 24:1603–1607CrossRefPubMedGoogle Scholar
  105. Rouxel O, Fouquet Y, Ludden JN (2004) Subsurface processes at the Lucky Strike hydrothermal field, Mid-Atlantic Ridge: evidence from sulfur, selenium, and iron isotopes. Geochim Cosmochim Ac 68:2295–2311CrossRefGoogle Scholar
  106. Schmaljohann R, Flügel HJ (1987) Methane-oxidizing bacteria in pogonophora. Sarsia 72:91–98Google Scholar
  107. Schulze A, Halanych KM (2003) Siboglinid evolution shaped by habitat preference and sulfide tolerance. Hydrobiologia 496(1–3):199–205CrossRefGoogle Scholar
  108. Scott KM (2003) A d13C-based carbon flux model for the hydrothermal vent chemoautotrophic symbiosis Riftia pachyptila predicts sizeable CO2 gradients at the host-symbiont interface. Environ Microbiol 5:424–432CrossRefPubMedGoogle Scholar
  109. Segel IH, Renosto F, PA Seubert (1987) Sulfate-activating enzymes. In: Jakoby WB, Griffith O (eds) Methods in enzymology, vol 143. Sulfur and sulfur amino acids. Academic Press, New York, pp 334–349Google Scholar
  110. Sibuet M, Olu K (1998) Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep Sea Res II 45:517–567CrossRefGoogle Scholar
  111. Sorgo A, Gaill F, Lechaire JP, Arndt C, Bright M (2002) Glycogen storage in the Riftia pachyptila trophosome: contribution of host and symbionts. Mar Ecol Prog Ser 231:115–120Google Scholar
  112. Stewart FJ, Newton ILG, Cavanaugh CM (2005) Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces. TRENDS Microbiol 13:439–448CrossRefPubMedGoogle Scholar
  113. Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99PubMedGoogle Scholar
  114. Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66:2898–2905CrossRefPubMedGoogle Scholar
  115. Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton Univ Press, Princeton, NJGoogle Scholar
  116. Van Dover CL, Fry B (1994) Microorganisms as food resources at deep-sea hydrothermal vents. Limnol Oceanog 39:51–57Google Scholar
  117. Van Dover CL, Lutz RA (2004) Experimental ecology at deep-sea hydrothermal vents: a perspective. J Exp Mar Biol Ecol 300: 273–307CrossRefGoogle Scholar
  118. Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81:569–628PubMedGoogle Scholar
  119. Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3:850–861CrossRefPubMedGoogle Scholar
  120. Zal F, Lallier FH, Wall JS, Vinogradov SN, Toulmond A (1996) The multihemoglobin system of the hydrothermal vent tube worm Riftia pachyptila.1. Reexamination of the number and masses of its constituents. J Biol Chem 271:8869–8874CrossRefPubMedGoogle Scholar
  121. Zal F, Suzuki T, Kawasaki Y, Childress JJ, Lallier FH, Toulmond A (1997) Primary structure of the common polypeptide chain b from the multi-hemoglobin system of the hydrothermal vent tube worm Riftia pachyptila: an insight on the sulfide binding-site. Proteins 29:562–574CrossRefPubMedGoogle Scholar
  122. Zal F, Leize E, Lallier FH, Toulmond A, Van Dorsselaer A, Childress JJ (1998) S-sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc Nat Acad Sci USA 95:8997–9002CrossRefPubMedGoogle Scholar
  123. Zhang JZ, Millero FJ (1993) The products from the oxidation of H2S in seawater. Geochim Cosmochim Ac 57:1705–1718CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2005

Authors and Affiliations

  • Frank J. Stewart
    • 1
  • Colleen M. Cavanaugh
    • 1
  1. 1.The Biological LaboratoriesDepartment of Organismic and Evolutionary Biology, Harvard UniversityCambridgeUSA

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