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Genetics and Evolution of Deep-Sea Chemosynthetic Bacteria and Their Invertebrate Hosts

  • Robert C. Vrijenhoek
Chapter
Part of the Topics in Geobiology book series (TGBI, volume 33)

Abstract

The clams, mussels, and tubeworms that dominate deep-sea chemosynthetic communities obtain most of their nutrition through intracellular symbiotic g-Proteobacteria that oxidize reduced compounds. The modes of symbiont transmission employed by various taxa have profound consequences for genetic, demographic, and evolutionary processes affecting the symbionts and their hosts. Vesicomyid clams transmit endosymbionts vertically via their eggs, a process that leads to symbiont clonality and accelerated rates of evolution. Vertical transmission provides the host with symbiont assurance because dispersing larvae carry the bacteria as they colonize new habitats. The symbionts and their host clams exhibit cospeciation. Vertical transmission for at least 45 million years has contributed to significant genome reduction, as the symbionts have lost almost half their DNA and many of the genes that were required for living in the ambient environment. In contrast, the horizontally transmitted symbionts associated with siboglinid tubeworms do not exhibit genome reduction. Tubeworm larvae are newly infected in each generation when they settle on appropriate substrates. Infection by local bacterial strains is hypothesized to provide the worms with locally optimal symbionts. Symbiont diversity is structured geographically and by habitat type (vent vs seep) and does not parallel host evolution. Less is known about the endosymbionts associated with various species of bathymodiolin mussels. Acquisition of local symbionts occurs in these mussels, but a vertical component of transmission might also exist. Symbiont diversity is structured geographically and not according to host species. The benefits of various symbiont transmission modes also carry associated risks that range from pure enslavement and genomic erosion under strictly vertical transmission to the possible evolution of bacterial strains that cheat the host when mixed symbiont genotypes infect a single host under horizontal transmission. The prevalence of horizontal transmission systems in chemosynthetic environments suggests that the symbionts must have escape strategies that allow them to ­re-inoculate the ambient environment and contribute to their overall fitness.

Keywords

Symbiosis Cospeciation Genome reduction Vestimentifera Vesicomyidae Bathymodiolinae 

Notes

Acknowledgements

I wish to thank the Frank Stewart, Shana Goffredi, Monika Bright, Julie Robidart, Steffen Kiel, Julio Harvey, Shannon Johnson and an anonymous reviewer for providing information and criticisms that improved the scope of this manuscript. Funding was provided by grants from the David and Lucile Packard Foundation to the Monterey Bay Research Institute and the National Science Foundation (OCE 0241613).

References

  1. Amano K, Kiel S (2007) Fossil vesicomyid bivalves from the North Pacific region. Veliger 49:270–293Google Scholar
  2. Amano K, Jenkins RG, Kurihara Y, Kiel S (2008) A new genus for Vesicomya inflata Kanie & Nishida, a lucinid shell convergent with that of vesicomyids, from Cretaceous strata of Hokkaido, Japan. Veliger 50:255–262Google Scholar
  3. Andersson SGE (2006) The bacterial world gets smaller. Science 314:259–260Google Scholar
  4. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) Genetics of colonizing species. Academic, New York, pp 147–172Google Scholar
  5. Barry JP, Greene HG, Orange DL, Baxter CH, Robison BH, Kochevar RE, Nybakken JW, Reed DL, McHugh CM (1996) Biologic and geologic characteristics of cold seeps in Monterey Bay, California. Deep Sea Res I 43:1739–1762Google Scholar
  6. Beijerinck MW (1913) Jaarboek van de Koninklijke Akademie v. Wetenschoppen. Muller, Amsterdam, The NetherlandsGoogle Scholar
  7. Belotte D, Curien J-B, Maclean RC, Bell G (2003) An experimental test of local adaptation in soil bacteria. Evolution 57:27–36Google Scholar
  8. Bergstrom CT, Lachmann M (2003) The Red King effect: when the slowest runner wins the coevolutionary race. Proc Natl Acad Sci USA 100:593–598Google Scholar
  9. Berquist DC, Williams FM, Fisher CR (2000) Longevity record for deep-sea invertebrate. Nature 403:499–500Google Scholar
  10. Birky CWJ, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513–527Google Scholar
  11. Birky CW Jr, Fuerst P, Maruyama T (1989) Organelle diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627Google Scholar
  12. Black MB, Halanych KM, Maas PAY, Hoeh WR, Hashimoto J, Desbruyères D, Lutz RA, Vrijenhoek RC (1997) Molecular systematics of vestimentiferan tube worms from hydrothermal vents and cold-water seeps. Mar Biol 130:141–149Google Scholar
  13. Blattner FR, Plunkett G III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462Google Scholar
  14. Boss KJ, Turner RD (1980) The giant white clam from the Galápagos rift, Calyptogena magnifica species novum. Malacologia 20:161–194Google Scholar
  15. Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC (2007) Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Res I 54:1773–1791Google Scholar
  16. Bright M, Giere O (2005) Microbial symbiosis in Annelida. Symbiosis 38:1–45Google Scholar
  17. Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci USA 90:5695–5699Google Scholar
  18. Cary SC, Felbeck H, Holland ND (1989) Observations on the reproductive biology of the hydrothermal vent tube worm Riftia pachyptila. Mar Ecol Prog Ser 52:89–94Google Scholar
  19. 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 Biotechnol 2:51–62Google Scholar
  20. Cary SC, Cottrell MT, Stein JT, Camacho F, Desbruyères D (1997) Molecular identification and localization of filamentous symbiotic bacteria associated with the hydrothermal vent annelid Alvinella pompejana. Appl Environ Microbiol 63:1124–1130Google Scholar
  21. Cavalier-Smith T, Lee JJ (1985) Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Eukaryot Microbiol 32:376–379Google Scholar
  22. 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 213:340–342Google Scholar
  23. Cavanaugh CM, McKinness AP, Newton ILG, Stewart FJ (2006) Marine chemosynthetic symbiosis. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 475–507Google Scholar
  24. Chevaldonné P, Jollivet D, Desbruyères D, Lutz RA, Vrijenhoek RC (2002) Sister-species of eastern Pacific hydrothermal-vent worms (Ampharetidae, Alvinelidae, Vestimentifera) provide new mitochondrial clock calibration. Cah Biol Mar 43:367–370Google Scholar
  25. Cho J-C, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66:5448–5456Google Scholar
  26. Clayton DH, Bush SE, Goates BM, Johnson KP (2003) Host defense reinforces host-parasite cospeciation. Proc Natl Acad Sci USA 100:15694–15699Google Scholar
  27. Corliss JB, Dymond J, Gordon LI, Edmond JM, Von Herzen RP, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, Van Andel TH (1979) Submarine thermal springs on the Galápagos Rift. Science 203:1073–1083Google Scholar
  28. DeChaine EG, Cavanaugh CM (2005) Symbioses of methanotrophs and deep-sea mussels (Mytilidae: Bathymodiolinae). In: Overmann J (ed) Progress in molecular and subcellular biology: molecular basis of symbiosis. Springer, Berlin, Heidelberg, pp 227–249Google Scholar
  29. 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 66:651–658Google Scholar
  30. Distel DL, Felbeck H, Cavanaugh CM (1994) Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts. J Mol Evol 38:533–542Google Scholar
  31. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680Google Scholar
  32. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434Google Scholar
  33. Downie JA, Young JPW (2001) Genome sequencing: the ABC of symbiosis. Nature 412:597–598Google Scholar
  34. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740Google Scholar
  35. Duperron S, Sibuet M, MacGregor BJ, Kuypers MMM, Fisher CR, 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 9:1423–1438Google Scholar
  36. Duperron S, Laurent MCZ, Gaill F, Gros O (2008a) Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol Ecol 63:338–349Google Scholar
  37. Duperron S, Halary S, Lorion J, Sibuet M, Gaill F (2008b) Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ Microbiol 10:433–445Google Scholar
  38. Elsaied H, Kimura H, Naganuma T (2002) Molecular characterization and endosymbiotic localization of the gene encoding D-ribulose 1, 5-bisphosphate carboxylase–oxygenase (RuBisCO) form II in the deep-sea vestimentiferan trophosome. Microbiology 148:1947–1957Google Scholar
  39. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630Google Scholar
  40. Endow K, Ohta S (1990) Occurrence of bacteria in the primary oocytes of vesicomyid clam Calyptogena soyoae. Mar Ecol Prog Ser 64:309–311Google Scholar
  41. Feldman RA, Black MB, Cary CS, Lutz RA, Vrijenhoek RC (1997) Molecular phylogenetics of bacterial endosymbionts and their vestimentiferan hosts. Mar Mol Biol Biotech 6:268–277Google Scholar
  42. Fisher CR, Brooks JM, Vodenichar JS, Zande JM, Childress JJ, Burke RA Jr (1993) The ­co-occurance of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar Ecol 14:277–289Google Scholar
  43. Frank SA (1996) Host-symbiont conflict over mixing of symbiotic lineages. Proc R Soc Lond B 263:33–344Google Scholar
  44. Frean MR, Abraham ER (2004) Adaptation and enslavement in endosymbiont-host associations. Phys Rev E 69:051913Google Scholar
  45. Freytag JK, Girguis PR, Bergquist DC, Andras JP, Childress JJ, Fisher CR (2001) A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc Natl Acad Sci USA 98:13408–13413Google Scholar
  46. Funk DJ, Helbling L, Wernegreen JJ, Moran NA (2000) Intraspecific phylogenetic congruence among multiple symbiont genomes. Proc R Soc Lond B 267:2517–2521Google Scholar
  47. Genkai-Kato M, Yamamura N (1999) Evolution of mutualistic symbiosis without vertical transmission. Theor Popul Biol 55:309–323Google Scholar
  48. Goffredi SK, Hurtado LA, Hallam S, Vrijenhoek RC (2003) Evolutionary relationships of deep-sea vent and seep clams (Mollusca: Vesicomyidae) of the ‘pacifica/lepta’ species complex. Mar Biol 142:311–320Google Scholar
  49. Goffredi SK, Warén A, Orphan VJ, Van Dover CL, Vrijenhoek RC (2004) Novel forms of structural integration between microbes and a vent gastropod from the Indian Ocean. Appl Environ Microbiol 70:3082–3090Google Scholar
  50. Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC (2008) Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ Microbiol 10:2623–2634Google Scholar
  51. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481Google Scholar
  52. Gros O, Darrasse A, Durand P, Frenkiel L, Moueza M (1996) Environmental transmission of sulfur-oxidizing bacterial gill endosymbiont in the tropical lucinid bivalve Codakia orbicularis. Appl Environ Microbiol 62:2324–2330Google Scholar
  53. Gros O, Frenkiel L, Moueza M (1998) Gill filament differentiation and experimental colonization by symbiotic bacteria in aposymbiotic juveniles of Codakia orbicularis (Bivalvia: Lucinidae). Invertebr Reprod Dev 34:219–231Google Scholar
  54. Hafner MS, Nadler SA (1988) Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332:258–259Google Scholar
  55. Harmer TL, Rotjan RD, Nussbaumer AD, Bright M, Ng AW, DeChaine EG, Cavanaugh CM (2008) Free-living tube worm endosymbionts found at deep-sea vents. Appl Environ Microbiol 74:3895–3898Google Scholar
  56. Harvey RW, Garabedian SP (1991) Use of colloid filtration theory in modeling movement of bacteria through a contaminated sandy aquifer. Environ Sci Technol 25:178–185Google Scholar
  57. Herry A, Le Pennec M (1986) Ultrastructure de la gonade d’un Mytilidae hydrothermal profond de la ride du Pacifique oriental. Haliotis 16:295–307Google Scholar
  58. Huelsenbeck JP, Rannala B, Yang Z (1997) Statistical tests of host-parasite cospeciation. Evolution 51:410–419Google Scholar
  59. Hurst GDD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B 272:1525–1534Google Scholar
  60. Hurtado LA, Mateos M, Lutz RA, Vrijenhoek RC (2003) Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl Environ Microbiol 69:2058–2064Google Scholar
  61. Jiggins FM, JHGvd S, Hurst GDD, Majerus MEN (2001) Recombination confounds interpretations of Wolbachia evolution. Proc R Soc Lond B 268:1423–1427Google Scholar
  62. Jones ML (1981) Riftia pachyptila, new genus, new species, the vestimentiferan worm from the Galápagos Rift geothermal vents (Pogonophora). Proc Biol Soc Wash 93:1295–1313Google Scholar
  63. Jones WJ, Vrijenhoek RC (2006) Evolutionary relationships within the “Bathymodiolus” childressi group. Cah Biol Mar 47:403–407Google Scholar
  64. Jones WJ, Won YJ, Maas PAY, Smith PJ, Lutz RA, Vrijenhoek RC (2006) Evolution of habitat use by deep-sea mussels. Mar Biol 148:841–851Google Scholar
  65. Kádár E, Bettencourt R, Costa V, Serrão Santos R, Lobo-da-Cunha A, Dando P (2005) Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. J Exp Mar Biol Ecol 318:99–110Google Scholar
  66. Kanie Y, Nishida T (2000) New species of chemosynthetic bivalves, Vesicomya and Acharax, from the Cretaceous deposits of northwestern Hokkaido. Sci Rep Yokosuka City Mus 47:79–84Google Scholar
  67. Kanie Y, Yoshikawa Y, Sakai T, Takahash T (1993) The Cretaceous chemosynthetic cold water-dependent molluscan community discovered from Mikasa City, Central Hokkaido. Sci Rep Yokosuka City Mus 41:31–132Google Scholar
  68. Kenk VC, Wilson BR (1985) A new mussel (Bivalvia, Mytilidae) from hydrothermal vents in the Galápagos Rift zone. Malacologia 26:253–271Google Scholar
  69. Kiel S, Dando PR (2009) Chaetopterid tubes from vent and seep sites: implications for fossil record and evolutionary history. Acta Palaeontol Pol 54(3):443–448Google Scholar
  70. Kiel S, Amano K, Jenkins RG (2008) Bivalves from Cretaceous cold-seep deposits on Hokkaido, Japan. Acta Palaeontol Pol 53:525–537Google Scholar
  71. Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425:78–81Google Scholar
  72. Krueger DM, Gustafson RG, Cavanaugh CM (1996) Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol Bull 190:195–202Google Scholar
  73. Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M, Matsuyama K, Takishita K, Kawato M, Uematsu K, Fujiwara Y, Sato T, Kato C, Kitagawa M, Kato I, Maruyama T (2007) Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol 17:881–886Google Scholar
  74. Lalou C, Brichet E (1982) Ages and implications of East Pacific Rise sulfide deposits at 21°N. Nature 300:169–171Google Scholar
  75. Lalou C, Reyss J-L, Brichet E, Arnold M, Thompson G, Fouquet Y, Rona P (1993) New age data for Mid-Atlantic Ridge hydrothermal sites: TAG and Snakepit chronology revisited. J Geophys Res 98:9705–9713Google Scholar
  76. Lambert JD, Moran NA (1998) Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95:4458–4462Google Scholar
  77. Le Pennec M, Diouris M, Herry A (1988) Endocytosis and lysis of bacteria in gill epithelium of Bathymodiolus thermophilus, Thyasira flexuosa and Lucinella divaricata (Bivalve, Molluscs). J Shell Res 7:483–489Google Scholar
  78. Little CTS, Vrijenhoek RC (2003) Are hydrothermal vent animals living fossils? Trends Ecol Evol 18:582–588Google Scholar
  79. Little CTS, Danelian T, Herrington RJ, Haymon R (2004) Early Jurassic hydrothermal vent ­community from the Franciscan complex, California. J Paleontol 78:542–559Google Scholar
  80. Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, Hugler M, Albrecht D, Robidart J, Bench S, Feldman RA, Hecker M, Schweder T (2007) Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315:247–250Google Scholar
  81. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favorable gene. Gene Res (Camb) 23:23–35Google Scholar
  82. McMullin E, Hourdez S, Schaeffer SW, Fisher CR (2003) Phylogeny and biogeography of deep sea vestimentiferans and their bacterial symbionts. Symbiosis 34:1–41Google Scholar
  83. Micheli F, Peterson CH, Mullineaux LS, Fisher CR, Mills SW, Sancho G, Johnson GA, Lenihan HS (2002) Predation structures communities at deep-sea hydrothermal vents. Ecol Monogr 72:365–382Google Scholar
  84. Moran NA (1996) Accelerated evolution and Muller’s ratchet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93:2873–2878Google Scholar
  85. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583–586Google Scholar
  86. Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond B 253:167–171Google Scholar
  87. Moran NA, McLaughlin HJ, Sorek R (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379–382Google Scholar
  88. Moya A, Pereto J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9:218–229Google Scholar
  89. Muller HJ (1964) The relation of mutation to mutational advance. Mutat Res 1:2–9Google Scholar
  90. Naganuma T, Naka J, Okayama Y, Minami A, Horikoshi K (1997) Morphological diversity of the microbial population in a vestimentiferan tubeworm. J Mar Biotech 53:193–197Google Scholar
  91. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267Google Scholar
  92. 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 vent habitats. CRC Press, Boca Raton, FL, pp 125–167Google Scholar
  93. Nelson K, Fisher CR (2000) Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbionts. Symbiosis 28:1–15Google Scholar
  94. Nelson DC, Waterbury JB, Jannasch HW (1984) DNA base composition and genome size of the prokaryotic symbiont in Riftia pachyptila (Pogonophora). FEMS Microbiol Lett 24:267–271Google Scholar
  95. Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM (2007) The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315:998–1000Google Scholar
  96. Newton ILG, Girguis PR, Cavanaugh CM (2008) Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts. BMC Genomics 9:585Google Scholar
  97. Nieberding CM, Durette-Desset M-C, Vanderpoorten A, Casanova JC, Ribas A, Deffontaine V, Feliu C, Morand S, Libois R, Michaux JR (2008) Geography and host biogeography matter for understanding the phylogeography of a parasite. Mol Phylogenet Evol 47:538–554Google Scholar
  98. Nishiguchi MK, Ruby EG, McFall-Ngai MJ (1998) Competitive dominance among strains of luminous bacteria provides an unusual evidence for parallel evolution in sepiolid squid-vibrio symbioses. Appl Environ Microbiol 64:3209–3213Google Scholar
  99. Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348Google Scholar
  100. Nyholm SV, McFall-Ngai MJ (2004) The winnowing: establishing the squid–Vibrio symbiosis. Nat Rev Microbiol 2:632–642Google Scholar
  101. O’Mullan GD, Maas PAY, Lutz RA, Vrijenhoek RC (2001) A hybrid zone between hydrothermal vent mussels (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Mol Ecol 10:2819–2831Google Scholar
  102. Ohta T (1987) Very slightly deleterious mutations and the molecular clock. J Mol Evol 26:1–6Google Scholar
  103. Page HM, Fisher CR, Childress JJ (1990) Role of filter-feeding in the nutritional biology of a deep-sea mussel with methanotrophic symbionts. Mar Biol 104:251–257Google Scholar
  104. Pailleret M, Haga T, Petit P, Prive-Gill C, Saedlou N, Gaill F, Zbinden M (2007) Sunken wood from the Vanuatu Islands: identification of wood substrates and preliminary description of associated fauna. Mar Ecol 28:233–241Google Scholar
  105. Pál C, Papp B, Lercher MJ, Csermely P, Oliver SG, Hurst LD (2006) Chance and necessity in the evolution of minimal metabolic networks. Nature 440:667–670Google Scholar
  106. Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5:650–659Google Scholar
  107. Peek A, Gustafson R, Lutz R, Vrijenhoek R (1997) Evolutionary relationships of deep-sea hydrothermal vent and cold-water seep clams (Bivalvia: Vesicomyidae): results from the mitochondrial cytochrome oxidase subunit I. Mar Biol 130:151–161Google Scholar
  108. Peek AS, Vrijenhoek RC, Gaut BS (1998a) Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol 15:1514–1523Google Scholar
  109. Peek AS, Feldman RA, Lutz RA, Vrijenhoek RC (1998b) Cospeciation of chemoautotrophic bacteria and deep-sea clams. Proc Natl Acad Sci USA 95:9962–9966Google Scholar
  110. Perez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314:312–313Google Scholar
  111. Reid SD, Selander RK, Whittam TS (1999) Sequence diversity of flagellin (fliC) alleles in pathogenic Escherichia coli. J Bacteriol 181:153–160Google Scholar
  112. Rispe C, Moran NA (2000) Accumulation of deleterious mutations in endosymbionts: Muller’s ratchet with two levels of selection. Am Nat 156:425–441Google Scholar
  113. Robidart JC, Benc SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterl T, Allen EE, Felbeck H (2008) Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10:727–737Google Scholar
  114. Salerno JL, Macko SA, Hallam SJ, Bright M, Won Y-J, McKiness Z, Van Dover CL (2005) Characterization of symbiont populations in life-history stages of mussels from chemosynthetic environments. Biol Bull 208:145–155Google Scholar
  115. Schloter M, Lebuhn M, Heulin T, Hartmann A (2000) Ecology and evolution of bacterial microdiversity. FEMS Microbiol Rev 24:647–660Google Scholar
  116. 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 45:517–567Google Scholar
  117. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr Comp Biol 42:369–380Google Scholar
  118. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol Annu Rev 41:311–354Google Scholar
  119. Southward EC (1988) Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): implications for relationship between Vestimentifera and Pogonophora. J Mar Biol Assoc UK 68:465–487Google Scholar
  120. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA: DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849Google Scholar
  121. Stewart FJ, Cavanaugh CM (2009) Pyrosequencing analysis of endosymbiont population structure: co-occurrence of divergent symbiont lineages in a single vesicomyid host clam. Environ Microbiol 11(8):2136–2147Google Scholar
  122. Stewart FJ, Newton ILG, Cavanaugh CM (2005) Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces. Trends Microbiol 13:439–448Google Scholar
  123. Stewart FJ, Young CR, Cavanaugh CM (2008) Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol Biol Evol 25:673–687Google Scholar
  124. Stewart FJ, Young CR, Cavanaugh CM (2009) Evidence for homologous recombination in intracellular chemosynthetic clam symbionts. Mol Biol Evol 26:1391–1404Google Scholar
  125. Tamames J, Gil R, Latorre A, Pereto J, Silva F, Moya A (2007) The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol 7:181Google Scholar
  126. Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16:R1016–R1017Google Scholar
  127. Trask JL, Van Dover CL (1999) Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol Oceanogr 44:334–343Google Scholar
  128. Tunnicliffe V, McArthur AG, Mchugh D (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv Mar Biol 34:353–442Google Scholar
  129. Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbour epsilon- and gamma-proteobacterial endosymbionts. Environ Microbiol 7:750–754Google Scholar
  130. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295:1253–1257Google Scholar
  131. Van Dover CL, Ward ME, Scott JL, Underdown J, Anderson B, Gustafson C, Whalen M, Carnegie RB (2007) A fungal epizootic in mussels at a deep-sea hydrothermal vent. Mar Ecol 28:54–62Google Scholar
  132. Van Valen L (1973) A new evolutionary law. Evol Theor 1:1–30Google Scholar
  133. Vetter RD (1991) Symbiosis and the evolution of novel trophic strategies: thiotrophic organisms at hydrothermal vents. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge, MA, pp 219–245Google Scholar
  134. Vrijenhoek RC (1997) Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Hered 88:285–293Google Scholar
  135. Vrijenhoek RC, Duhaime M, Jones WJ (2007) Subtype variation among bacterial endosymbionts of tubeworms (Annellida: Siboglinidae) from the Gulf of California. Biol Bull 212:180–184Google Scholar
  136. Wernegreen JJ, Moran NA (1999) Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein coding genes. Mol Biol Evol 16:83–97Google Scholar
  137. Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic Archaea. Science 301:976–978Google Scholar
  138. Won Y-J, Hallam SJ, O’Mullan GD, Vrijenhoek RC (2003a) Cytonuclear disequilibrium in a hybrid zone involving deep-sea hydrothermal vent mussels of the genus Bathymodiolus. Mol Ecol 12:3185–3190Google Scholar
  139. Won Y-J, Hallam SJ, O’Mullan GD, Pan IL, Buck KR, Vrijenhoek RC (2003b) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl Environ Microbiol 69:6785–6792Google Scholar
  140. Won Y-J, Jones WJ, Vrijenhoek RC (2008) Absence of co-speciation between deep-sea mytilids and their thiotrophic endosymbionts. J Shell Res 27:129–138Google Scholar
  141. Young CR, Fujio S, Vrijenhoek RC (2008) Directional dispersal between mid-ocean ridges: deep-ocean circulation and gene flow in Ridgeia piscesae. Mol Ecol 17:1718–1731Google Scholar
  142. Zbinden M, Shillito B, Le Bris N, de Villardi de Montlaur C, Roussel E, Guyot F, Gaill F, Cambon-Bonavita M-A (2008) New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J Exp Mar Biol Ecol 359:131–140Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Monterey Bay Aquarium Research InstituteMoss LandingUSA

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