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  • Review Article
  • Published:

Symbiotic diversity in marine animals: the art of harnessing chemosynthesis

Nature Reviews Microbiology volume 6, pages 725–740 (2008)Cite this article

Key Points

  • Chemosynthetic symbioses between bacteria and marine invertebrates were discovered 30 years ago at hydrothermal vents on the Galapagos Rift. Remarkably, it took the discovery of these symbioses in the deep sea for scientists to realize that chemosynthetic symbioses occur worldwide in a wide range of habitats, including cold seeps, whale and wood falls, shallow-water coastal sediments and continental margins.

  • The most well known habitats for chemosynthetic symbioses are those in the deep sea. Deep-sea hydrothermal vents were the first habitats to be discovered in which chemosynthetic rather than photosynthetic primary production fuels large animal communities that are considered to belong to some of the most productive on the Earth.

  • When organic matter falls to the deep-sea floor in the form of whale carcasses or sunken wood (named whale and wood falls), it supports chemosynthetic communities for limited periods of time.

  • Only at vents and seeps do these associations dominate the biomass and form large standing crops. At whale and wood falls, chemosynthetic symbioses form only a small part of the animal community.

  • A remarkable number of animals have established symbioses with chemosynthetic symbionts. The morphological diversity of chemosynthetic associations is also high, showing the adaptive flexibility of both the animals and the microorganisms in these associations. In addition to morphological diversity, the behavioural and physiological strategies used by animals to supply their symbionts with both reductants and oxidants vary markedly, even within closely related host groups.

  • Until recently, the diversity of chemosynthetic symbionts was considerably underestimated. Progress in the molecular techniques that have been used to detect microbial diversity has led to the realization that more than two endosymbionts can co-occur in both deep-sea and shallow-water hosts. Just as molecular analyses have led to the discovery of unrecognized phylogenetic diversity, genomic and proteomic analyses are beginning to reveal the metabolic diversity of chemosynthetic symbionts.

Abstract

Chemosynthetic symbioses between bacteria and marine invertebrates were discovered 30 years ago at hydrothermal vents on the Galapagos Rift. Remarkably, it took the discovery of these symbioses in the deep sea for scientists to realize that chemosynthetic symbioses occur worldwide in a wide range of habitats, including cold seeps, whale and wood falls, shallow-water coastal sediments and continental margins. The evolutionary success of these symbioses is evident from the wide range of animal groups that have established associations with chemosynthetic bacteria; at least seven animal phyla are known to host these symbionts. The diversity of the bacterial symbionts is equally high, and phylogenetic analyses have shown that these associations have evolved on multiple occasions by convergent evolution. This Review focuses on the diversity of chemosynthetic symbionts and their hosts, and examines the traits that have resulted in their evolutionary success.

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Figure 1: Chemosynthetic symbioses in different marine habitats.
Figure 2: Symbioses found at deep-sea hydrothermal vents.
Figure 3: Symbioses found both at deep-sea hydrothermal vents and cold seeps.
Figure 4: Symbioses in bivalves from shallow-water habitats.
Figure 5: Symbioses in worms and protists from shallow-water habitats.
Figure 6: Phylogenetic diversity of gammaproteobacterial, chemosynthetic symbionts based on their 16S ribosomal RNA gene sequences.

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References

  1. De Beer, G. The Pogonophora. Nature 176, 888 (1955).

    Article  Google Scholar 

  2. Southward, A. J., Southward, E. C., Brattegard, T. & Bakke, T. Further experiments on the value of dissolved organic matter as food for Siboglinum fiordicum (Pogonophora). J. Mar. Biolog. Assoc. UK 59, 133–148 (1979).

    Article  CAS  Google Scholar 

  3. Van Dover, C. L. The Ecology of Deep-Sea Hydrothermal Vents (Princeton Univ. Press, New Jersey, 2000). This book provides one of the most comprehensive and well written overviews of the ecology of hydrothermal vents.

    Google Scholar 

  4. Cavanaugh, C. M., McKiness, Z. P., Newton, I. L. G. & Stewart, F. J. in The Prokaryotes (eds Dworkin, M., Falkow, S. I., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) 475–507 (Springer, New York, 2006). This review provides an excellent overview of studies on chemosynthetic symbioses.

    Book  Google Scholar 

  5. McManus, R. You'd know a lot if you knew all the dirt. NIH Record [online] (2002).

  6. Smith, C. R. & Baco, A. R. in Oceanography and Marine Biology Vol. 41 (eds Gibson, R. N. & Atkinson, R. J. A.) 311–354 (Taylor & Francis, London, 2003).

    Google Scholar 

  7. Hentschel, U., Cary, S. C. & Felbeck, H. Nitrate respiration in chemoautotrophic symbionts of the bivalve Lucinoma aequizonata. Mar. Ecol. Prog. Ser. 94, 35–41 (1993).

    Article  CAS  Google Scholar 

  8. Girguis, P. R. et al. Fate of nitrate acquired by the tubeworm Riftia pachyptila. Appl. Environ. Microbiol. 66, 2783–2790 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Distel, D. L. et al. Do mussels take wooden steps to deep-sea vents? Nature 403, 725–726 (2000).

    Article  CAS  PubMed  Google Scholar 

  10. Duperron, S., Laurent, M. C. Z., Gaill, F. & Gros, O. Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol. Ecol. 63, 338–349 (2008).

    Article  CAS  PubMed  Google Scholar 

  11. Dando, P. R. et al. Shipwrecked tube worms. Nature 356, 667 (1992).

    Article  Google Scholar 

  12. Hughes, D. J. & Crawford, M. A new record of the vestimentiferan Lamellibrachia sp. (Polychaeta: Siboglinidae) from a deep shipwreck in the eastern Mediterranean. JMBA2 Biodiversity Records [online] (2006).

  13. Hashimoto, J., Miura, T., Fujikura, K. & Ossaka, J. Discovery of vestimentiferan tube worms in the euphotic zone. Zool. Sci. 10, 1063–1067 (1993).

    Google Scholar 

  14. Tarasov, V. G., Gebruk, A. V., Mironov, A. N. & Moskalev, L. I. Deep-sea and shallow-water hydrothermal vent communities: two different phenomena? Chem. Geol. 224, 5–39 (2005).

    Article  CAS  Google Scholar 

  15. Glover, A. G., Kallstrom, B., Smith, C. R. & Dahlgren, T. G. World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc. Biol. Sci. 272, 2587–2592 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dahlgren, T. G. et al. A shallow-water whale-fall experiment in the north Atlantic. Cah. Biol. Mar. 47, 385–389 (2006).

    Google Scholar 

  17. Fujiwara, Y. et al. Three-year investigations into sperm whale-fall ecosystems in Japan. Mar. Ecol. Evol. Persp. 28, 219–232 (2007).

    Article  Google Scholar 

  18. Little, C. T. S., Campbell, K. A. & Herrington, R. J. Why did ancient chemosynthetic seep and vent assemblages occur in shallower water than they do today? Int. J. Earth Sci. 91, 149–153 (2002).

    Article  Google Scholar 

  19. Reid, R. G. B. & Bernard, F. R. Gutless bivalves. Science 208, 609–610 (1980).

    Article  CAS  PubMed  Google Scholar 

  20. Durand, P., Gros, O., Frenkiel, L. & Prieur, D. Phylogenetic characterization of sulfur-oxidizing bacterial endosymbionts in three tropical Lucinidae by 16S rDNA sequence analysis. Mol. Marine Biol. Biotechnol. 5, 37–42 (1996).

    CAS  Google Scholar 

  21. Ott, J. A., Bright, M. & Schiemer, F. The ecology of a novel symbiosis between a marine peritrich ciliate and chemoautotrophic bacteria. Mar. Ecol. 19, 229–243 (1998).

    Article  CAS  Google Scholar 

  22. Rinke, C. et al. “Candidatus Thiobios zoothamnicoli”, an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl. Environ. Microbiol. 72, 2014–2021 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Blazejak, A., Erseus, C., Amann, R. & Dubilier, N. Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71, 1553–1561 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ruehland, C. et al. Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments. Environ. Microbiol. (in the press).

  25. Blazejak, A., Kuever, J., Erseus, C., Amann, R. & Dubilier, N. Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase, and adenosine 5 -phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl. Environ. Microbiol. 72, 5527–5536 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ott, J., Bright, M. & Bulgheresi, S. Symbioses between marine nematodes and sulfur-oxidizing chemoautotrophic bacteria. Symbiosis 36, 103–126 (2004).

    CAS  Google Scholar 

  27. Musat, N. et al. Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environ. Microbiol. 9, 1345–1353 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Krueger, D. M., Dubilier, N. & Cavanaugh, C. M. Chemoautotrophic symbiosis in the tropical clam Solemya occidentalis (Bivalvia: Protobranchia): ultrastructural and phylogenetic analysis. Mar. Biol. 126, 55–64 (1996).

    Article  Google Scholar 

  29. Glover, E. A. & Taylor, J. D. Diversity of chemosymbiotic bivalves on coral reefs: Lucinidae (Mollusca, Bivalvia) of New Caledonia and Lifou. Zoosystema 29, 109–181 (2007).

    Google Scholar 

  30. Taylor, J. D. & Glover, E. A. Lucinidae (Bivalvia) — the most diverse group of chemosymbiotic molluscs. Zool. J. Linn. Soc. 148, 421–438 (2006). This review describes the remarkable diversity of lucinid clams with chemosynthetic symbionts.

    Article  Google Scholar 

  31. Dubilier, N. et al. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411, 298–302 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Werner, U. et al. Spatial patterns of aerobic and anaerobic mineralization rates and oxygen penetration dynamics in coral reef sediments. Mar. Ecol. Prog. Ser. 309, 93–105 (2006).

    Article  CAS  Google Scholar 

  33. Ramirez-Llodra, E., Shank, T. M. & German, C. R. Biodiversity and biogeography of hydrothermal vent species: thirty years of discovery and investigations. Oceanography 20, 33–41 (2007).

    Article  Google Scholar 

  34. Jones, W. J., Johnson, S. B., Rouse, G. W. & Vrijenhoek, R. C. Marine worms (genus Osedax) colonize cow bones. Proc. Biol. Sci. 275, 387–391 (2008).

    Article  PubMed  Google Scholar 

  35. Palacios, C. et al. Microbial ecology of deep-sea sunken wood: quantitative measurements of bacterial biomass and cellulolytic activities. Cah. Biol. Mar. 47, 415–420 (2006).

    Google Scholar 

  36. Dufour, S. C. Gill anatomy and the evolution of symbiosis in the bivalve family Thyasiridae. Biol. Bull. 208, 200–212 (2005).

    Article  PubMed  Google Scholar 

  37. Erséus, C. A new species, Olavius ulrikae (Annelida: Clitellata: Tubificidae), re-assessment of a Western Australian gutless marine worm. Rec. West. Aust. Mus. 24, 195–198 (2008).

    Article  Google Scholar 

  38. Gros, O., Liberge, M. & Felbeck, H. Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Mar. Biol. 142, 57–66 (2003). The first paper to show that a host can acquire symbionts from other chemosynthetic host species.

    Article  Google Scholar 

  39. Distel, D. L. & Wood, A. P. Characterization of the gill symbiont of Thyasira flexuosa (Thyasiridae: Bivalvia) by use of polymerase chain reaction and 16S rRNA sequence analysis. J. Bacteriol. 174, 6317–6320 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dubilier, N., Blazejak, A. & Ruehland, C. in Progress in Molecular and Subcellular Biology Vol. 43 (eds Cimino, G. & Gavagnin, M.) 251–275 (Springer-Verlag, Berlin, 2006).

    Google Scholar 

  41. Kouris, A., Juniper, S. K., Frebourg, G. & Gaill, F. Protozoan–bacterial symbiosis in a deep-sea hydrothermal vent folliculinid ciliate (Folliculinopsis sp.) from the Juan de Fuca Ridge. Mar. Ecol. 28, 63–71 (2007).

    Article  Google Scholar 

  42. Fenchel, T. & Finlay, B. J. Kentrophores: a mouthless ciliate with a symbiotic kitchen garden. Ophelia 30, 75–93 (1989).

    Google Scholar 

  43. Fenchel, T. M. & Riedl, R. J. Sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar. Biol. 7, 255 (1970).

    Article  CAS  Google Scholar 

  44. Schmidt, C., Le Bris, N. & Gaill, F. Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J. Shellfish Res. 27, 79–90 (2008).

    Article  Google Scholar 

  45. Zbinden, M. et al. New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J. Exp. Mar. Biol. Ecol. 359, 131–140 (2008).

    Article  Google Scholar 

  46. Bright, M. & Giere, O. Microbial symbiosis in Annelida. Symbiosis 38, 1–45 (2005).

    Google Scholar 

  47. Duperron, S., Halary, S., Lorion, J., Sibuet, M. & Gaill, F. Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ. Microbiol. 10, 433–445 (2008).

    Article  CAS  PubMed  Google Scholar 

  48. Southward, E. C. The morphology of bacterial symbioses in the gills of mussels of the genera Adipicola and Idas (Bivalvia: Mytilidae). J. Shellfish Res. 27, 139–146 (2008).

    Article  Google Scholar 

  49. Samadi, S. et al. Molecular phylogeny in mytilids supports the wooden steps to deep-sea vents hypothesis. C. R. Biol. 330, 446–456 (2007).

    Article  CAS  PubMed  Google Scholar 

  50. Won, Y. J., Jones, W. J. & Vrijenhoek, R. C. Absence of cospeciation between deep-sea Mytilids and their thiotrophic endosymbionts. J. Shellfish Res. 27, 129–138 (2008).

    Article  Google Scholar 

  51. Duperron, S. et al. Symbioses between deep-sea mussels (Mytilidae: Bathymodiolinae) and chemosynthetic bacteria: diversity, function and evolution. C. R. Acad. Sci. Biol. (in the press).

  52. Southward, E. C., Schulze, A. & Gardiner, S. L. Pogonophora (Annelida): form and function. Hydrobiologia 535, 227–251 (2005).

    Google Scholar 

  53. Nussbaumer, A. D., Fisher, C. R. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345–348 (2006). A study of the acquisition of symbionts in vent tube worms with first-rate ultrastructural and FISH analyses.

    Article  CAS  PubMed  Google Scholar 

  54. Goffredi, S. K. et al. Evolutionary innovation: a bone-eating marine symbiosis. Environ. Microbiol. 7, 1369–1378 (2005).

    Article  CAS  PubMed  Google Scholar 

  55. Rouse, G. W., Goffredi, S. K. & Vrijenhoek, R. C. Osedax: bone-eating marine worms with dwarf males. Science 305, 668–671 (2004). The first paper to describe the gutless siboglinid worms that colonize whale bones.

    Article  CAS  PubMed  Google Scholar 

  56. Zal, F. et al. S-sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc. Natl Acad. Sci. USA 95, 8997–9002 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hahlbeck, E., Pospesel, M. A., Zal, F., Childress, J. J. & Felbeck, H. Proposed nitrate binding by hemoglobin in Riftia pachyptila blood. Deep Sea Res. Part I 52, 1885–1895 (2005).

    Article  Google Scholar 

  58. Flores, J. F. et al. Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc. Natl Acad. Sci. USA 102, 2713–2718 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Cordes, E. E., Arthur, M. A., Shea, K., Arvidson, R. S. & Fisher, C. R. Modeling the mutualistic interactions between tubeworms and microbial consortia. PloS Biol. 3, 497–506 (2005).

    Article  CAS  Google Scholar 

  60. Ott, J. A. et al. Tackling the sulfide gradient: a novel strategy involving marine nematodes and chemoautotrophic ectosymbionts. Mar. Ecol. 12, 261–279 (1991).

    Article  Google Scholar 

  61. Childress, J. J., Fisher, C. R., Favuzzi, J. A. & Sanders, N. K. Sulfide and carbon-dioxide uptake by the hydrothermal vent clam, Calyptogena magnifica, and its chemoautotrophic symbionts. Physiol. Zool. 64, 1444–1470 (1991).

    Article  CAS  Google Scholar 

  62. Zal, F. et al. Haemoglobin structure and biochemical characteristics of the sulphide-binding component from the deep-sea clam Calyptogena magnifica. Cah. Biol. Mar. 41, 413–423 (2000).

    Google Scholar 

  63. Doeller, J. E., Kraus, D. W., Colacino, J. M. & Wittenberg, J. B. Gill hemoglobin may deliver sulfide to bacterial symbionts of Solemya velum (Bivalvia, Mollusca). Biol. Bull. 175, 388–396 (1988).

    Article  CAS  Google Scholar 

  64. Johnson, K. S., Childress, J. J., Beehler, C. L. & Sakamoto, C. M. Biogeochemistry of hydrothermal vent mussel communities: the deep-sea analog to the intertidal zone. Deep Sea Res. Part I 41, 993–1011 (1994). A seminal study on the interactions between vent biota and biogeochemistry.

    Article  CAS  Google Scholar 

  65. Dufour, S. C. & Felbeck, H. Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426, 65–67 (2003).

    Article  CAS  PubMed  Google Scholar 

  66. Stahl, D. A., Lane, D. J., Olsen, G. J. & Pace, N. R. Analysis of hydrothermal vent-associated symbionts by rRNA sequences. Science 224, 409–411 (1984).

    Article  CAS  PubMed  Google Scholar 

  67. Distel, D. L. et al. Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J. Bacteriol. 170, 2506–2510 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Nakagawa, S. & Takai, K. Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol. Ecol. 65, 1–14 (2008).

    Article  CAS  PubMed  Google Scholar 

  69. Polz, M. F. & Cavanaugh, C. M. Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proc. Natl Acad. Sci. USA 92, 7232–7236 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Haddad, A., Camacho, F., Durand, P. & Cary, S. C. Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl. Environ. Microbiol. 61, 1679–1687 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Cary, S. C., Cottrell, M. T., Stein, J. L., Camacho, F. & Desbruyeres, D. Molecular identification and localization of filamentous symbiotic bacteria associated with the hydrothermal vent annelid Alvinella pompejana. Appl. Environ. Microbiol. 63, 1124–1130 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Urakawa, H. et al. Hydrothermal vent gastropods from the same family (Provannidae) harbour e- and g-proteobacterial endosymbionts. Environ. Microbiol. 7, 750–754 (2005).

    Article  CAS  PubMed  Google Scholar 

  73. Suzuki, Y. et al. Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl. Environ. Microbiol. 71, 5440–5450 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Distel, D. L. & Cavanaugh, C. M. Independent phylogenetic origins of methanotrophic and chemoautotrophic bacterial endosymbioses in marine bivalves. J. Bacteriol. 176, 1932–1938 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Borowski, C., Giere, O., Krieger, J., Amann, R. & Dubilier, N. New aspects of the symbiosis in the provannid snail Ifremeria nautilei from the North Fiji Back Arc Basin. Cah. Biol. Mar. 43, 321–324 (2002).

    Google Scholar 

  76. Schmaljohann, R. & Flugel, H. J. Methane-oxidizing bacteria in Pogonophora. Sarsia 72, 91–99 (1987).

    Article  CAS  Google Scholar 

  77. Pimenov, N. V., Savvichev, A. S., Rusanov, I. I., Lein, A. Y. & Ivanov, M. V. Microbiological processes of the carbon and sulfur cycles at cold methane seeps of the North Atlantic. Mikrobiologiia 69, 709–720 (2000).

    CAS  Google Scholar 

  78. Lösekann, T. et al. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an arctic cold seep (Haakon Mosby Mud Volcano, Barents Sea). Environ. Microbiol. 14 Aug 2008 (doi:10.1111/j.1462-2920.2008.01712.x).

    Article  CAS  PubMed  Google Scholar 

  79. Fisher, C. R. et al. The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar. Ecol. 14, 277–289 (1993). The first detailed description of a dual symbiosis in a chemosynthetic host.

    Article  Google Scholar 

  80. Distel, D. L., Lee, H. K.-W. & Cavanaugh, C. M. Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc. Natl Acad. Sci. USA 92, 9598–9602 (1995). The first study to show that two bacterial symbionts can coexist within the same metazoan host cell.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Duperron, S. et al. 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. 8, 1441–1447 (2006).

    Article  CAS  PubMed  Google Scholar 

  82. Suzuki, Y. et al. Single host and symbiont lineages of hydrothermal-vent gastropods Ifremeria nautilei (Provannidae): biogeography and evolution. Mar. Ecol. 315, 167–175 (2006).

    Article  CAS  Google Scholar 

  83. Duperron, S. et al. 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, 1423–1438 (2007).

    Article  CAS  PubMed  Google Scholar 

  84. Campbell, B. J. & Cary, S. C. Characterization of a novel spirochete associated with the hydrothermal vent polychaete annelid, Alvinella pompejana. Appl. Environ. Microbiol. 67, 110–117 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Nelson, K. & Fisher, C. R. Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbionts. Symbiosis 28, 1–15 (2000).

    Google Scholar 

  86. Vrijenhoek, R. C., Duhaime, M. & Jones, W. J. Subtype variation among bacterial endosymbionts of tubeworms (Annelida: Siboglinidae) from the Gulf of California. Biol. Bull. 212, 180–184 (2007).

    Article  CAS  PubMed  Google Scholar 

  87. Di Meo, C. A. et al. Genetic variation among endosymbionts of widely distributed vestimentiferan tubeworms. Appl. Environ. Microbiol. 66, 651–658 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Won, Y. J. et al. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl. Environ. Microbiol. 69, 6785–6792 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. DeChaine, E. G., Bates, A. E., Shank, T. M. & Cavanaugh, C. M. Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ. Microbiol. 8, 1902–1912 (2006).

    Article  CAS  PubMed  Google Scholar 

  90. Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Robidart, J. C. et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727–737 (2008).

    Article  CAS  PubMed  Google Scholar 

  92. Harmer, T. L. et al. Free-living tube worm endosymbionts found at deep-sea vents. Appl. Environ. Microbiol. 74, 3895–3898 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Markert, S. et al. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315, 247–250 (2007). This paper provides the first evidence that a chemoautotrophic symbiont uses two different pathways to fix inorganic carbon depending on its energy store.

    Article  CAS  PubMed  Google Scholar 

  94. Moya, A., Pereto, J., Gil, R. & Latorre, A. Learning how to live together: genomic insights into prokaryote–animal symbioses. Nature Rev. Genet. 9, 218–229 (2008). An excellent overview of symbioses between animals and microorganisms that particularly focused on insect symbioses.

    Article  CAS  PubMed  Google Scholar 

  95. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev. Microbiol. 6, 776–788 (2008).

    Article  CAS  Google Scholar 

  96. Peek, A. S., Feldman, R. A., Lutz, R. A. & Vrijenhoek, R. C. Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc. Natl Acad. Sci. USA 95, 9962–9966 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Goffredi, S. K., Hurtado, L. A., Hallam, S. & Vrijenhoek, R. C. Evolutionary relationships of deep-sea vent and cold seep clams (Mollusca: Vesicomyidae) of the “pacifica/lepta” species complex. Mar. Biol. 142, 311–320 (2003).

    Article  Google Scholar 

  98. Hurtado, L. A., Mateos, M., Lutz, R. A. & Vrijenhoek, R. C. Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl. Environ. Microbiol. 69, 2058–2064 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Stewart, F. J., Young, C. R. & Cavanaugh, C. M. Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol. Biol. Evol. 25, 673–687 (2008).

    Article  CAS  PubMed  Google Scholar 

  100. 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. 69, 6264–6267 (2003). The first study to provide evidence for a free-living stage of a chemosynthetic symbiont.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Kadar, E. et al. Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus. J. Exp. Mar. Biol. Ecol. 318, 99–110 (2005).

    Article  Google Scholar 

  102. Giere, O. & Langheld, C. Structural organization, transfer and biological fate of endosymbiotic bacteria in gutless oligochaetes. Mar. Biol. 93, 641–650 (1987).

    Article  Google Scholar 

  103. Moran, N. A. Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl Acad. Sci. USA 104, 8627–8633 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kojima, S., Segawa, R., Fujiwara, Y., Hashimoto, J. & Ohta, S. Genetic differentiation of populations of a hydrothermal vent-endemic gastropod, Ifremeria nautilei, between the North Fiji Basin and the Manus Basin revealed by nucleotide sequences of mitochondrial DNA. Zool. Sci. 17, 1167–1174 (2000).

    Article  CAS  Google Scholar 

  105. Little, C. T. S. & Vrijenhoek, R. C. Are hydrothermal vent animals living fossils? Trends Ecol. Evol. 18, 582–588 (2003). An excellent review of the fossil record of chemosynthetic hosts.

    Article  Google Scholar 

  106. Herre, E. A., Knowlton, N., Mueller, U. G. & Rehner, S. A. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14, 49–53 (1999).

    Article  CAS  PubMed  Google Scholar 

  107. West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672 (2007).

    Article  CAS  PubMed  Google Scholar 

  108. McFall-Ngai, M. J. The development of cooperative associations between animals and bacteria: establishing détente among domains. Am. Zool. 38, 593–608 (1998).

    Article  CAS  Google Scholar 

  109. Trask, J. L. & Van Dover, C. L. Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol. Oceanogr. 44, 334–343 (1999).

    Article  Google Scholar 

  110. Halary, S., Riou, V., Gaill, F., Boudier, T. & Duperron, S. 3D FISH for the quantification of methane- and sulphur-oxidizing endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus. ISME J. 2, 284–292 (2008).

    Article  CAS  PubMed  Google Scholar 

  111. Fisher, C. R. in Biogeochemistry of Global Change: Radiatively Active Trace Gases (ed. Oremland, R. S.) 606–618 (Chapman & Hall, London, 1993).

    Book  Google Scholar 

  112. Nauhaus, K., Albrecht, M., Elvert, M., Boetius, A. & Widdel, F. In vitro cell growth of marine archaeal–bacterial consortia during anaerobic oxidation of methane with sulfate. Environ. Microbiol. 9, 187–196 (2007).

    Article  CAS  PubMed  Google Scholar 

  113. Dubilier, N. The searchlight and the bucket of microbial ecology. Environ. Microbiol. 9, 2–3 (2007).

    Article  PubMed  Google Scholar 

  114. Sipos, R. et al. Effect of primer mismatch, annealing temperature and PCR cycle number on 16S rRNA gene-targetting bacterial community analysis. FEMS Microbiol. Ecol. 60, 341–350 (2007).

    Article  CAS  PubMed  Google Scholar 

  115. Acinas, S. G., Sarma-Rupavtarm, R., Klepac-Ceraj, V. & Polz, M. F. PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl. Environ. Microbiol. 71, 8966–8969 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Amann, R. & Fuchs, B. M. Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Rev. Microbiol. 6, 339–348 (2008).

    Article  CAS  Google Scholar 

  117. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Moran, N. A. Tracing the evolution of gene loss in obligate bacterial symbionts. Curr. Opin. Microbiol. 6, 512–518 (2003). Papers by this author are worth reading for their clarity, high quality and thought-provoking ideas.

    Article  CAS  PubMed  Google Scholar 

  119. Hosokawa, T., Kikuchi, Y., Nikoh, N., Shimada, M. & Fukatsu, T. Strict host–symbiont cospeciation and reductive genome evolution in insect gut bacteria. PloS Biol. 4, 1841–1851 (2006). This paper provides an example of genome reduction in a horizontally transmitted symbiont.

    Article  CAS  Google Scholar 

  120. Newton, I. L. G. et al. The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315, 998–1000 (2007).

    Article  CAS  PubMed  Google Scholar 

  121. Kuwahara, H. et al. Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr. Biol. 17, 881–886 (2007).

    Article  CAS  PubMed  Google Scholar 

  122. Kuwahara, H. et al. Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams. Extremophiles 12, 365–374 (2008).

    Article  CAS  PubMed  Google Scholar 

  123. Plague, G. R., Dunbar, H. E., Tran, P. L. & Moran, N. A. Extensive proliferation of transposable elements in heritable bacterial symbionts. J. Bacteriol. 190, 777–779 (2008).

    Article  CAS  PubMed  Google Scholar 

  124. Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188–7196 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Desbruyères, D., Segonzac, M. & Bright, M. Handbook of Deep-Sea Hydrothermal Vent Fauna (eds Desbruyères, D., Segonzac, M. & Bright, M.) (Biologiezentrum der Oberösterreichischen Landesmuseen: Linz, Austria, 2006). The definitive handbook on the biology and geography of hydrothermal-vent animals.

    Google Scholar 

  126. Görtz, H.-D. in The Prokaryotes (eds Dworkin, M., Falkow, S. I., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) 364–402 (Springer, New York, 2006).

    Book  Google Scholar 

  127. Vacelet, J. & Boury-Esnault, N. A new species of carnivorous deep-sea sponge (Demospongiae: Cladorhizidae) associated with methanotrophic bacteria. Cah. Biol. Mar. 43, 141–148 (2002).

    Google Scholar 

  128. Gruber, H. & Ott, J. Localization of sulfur in the symbionts of a rectronectid plathelminth by EDX and EFTEM. 40th European Marine Biology Symposium, 101 (2005).

  129. Ott, J., Rieger, G., Rieger, R. & Enderes, F. New mouthless interstitial worms from the sulfide system symbiosis with prokaryotes. Mar. Ecol. 3, 313–334 (1982).

    Article  Google Scholar 

  130. Nussbaumer, A. D., Bright, M., Baranyi, C., Beisser, C. J. & Ott, J. A. Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes. Aquat. Microb. Ecol. 34, 239–246 (2004). The first paper to suggest that lectins are important for the binding of chemosynthetic episymbionts to the surface of their host.

    Article  Google Scholar 

  131. Katz, S., Cavanaugh, C. M. & Bright, M. Symbiosis of epi- and endocuticular bacteria with Helicoradomenia spp. (Mollusca, Aplacophora, Solenogastres) from deep-sea hydrothermal vents. Mar. Ecol. Prog. Ser. 320, 89–99 (2006).

    Article  Google Scholar 

  132. Duperron, S., Fiala-Medioni, A., Caprais, J. C., Olu, K. & Sibuet, M. Evidence for chemoautotrophic symbiosis in a Mediterranean cold seep clam (Bivalvia: Lucinidae): comparative sequence analysis of bacterial 16S rRNA, APS reductase and RubisCO genes. FEMS Microbiol. Ecol. 59, 64–70 (2007).

    Article  CAS  PubMed  Google Scholar 

  133. Fujiwara, Y., Kato, C., Masui, N., Fujikura, K. & Kojima, S. Dual symbiosis in the cold-seep thyasirid clam Maorithyas hadalis from the hadal zone in the Japan Trench, western Pacific. Mar. Ecol. Prog. Ser. 214, 151–159 (2001).

    Article  Google Scholar 

  134. Suzuki, Y. et al. Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host–animal type: the genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol. Lett. 249, 105–112 (2005).

    Article  CAS  PubMed  Google Scholar 

  135. Bates, A. E. Feeding strategy, morphological specialisation and presence of bacterial episymbionts in lepetodrilid gastropods from hydrothermal vents. Mar. Ecol. Prog. Ser. 347, 87–99 (2007).

    Article  Google Scholar 

  136. Goffredi, S. K., Waren, A., Orphan, V. J., Van Dover, C. L. & Vrijenhoek, R. C. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70, 3082–3090 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Halanych, K. M. Molecular phylogeny of siboglinid annelids (a.k.a. pogonophorans): a review. Hydrobiologia 535, 297–307 (2005).

    Google Scholar 

  138. Feldman, R. A. et al. Vestimentiferan on a whale fall. Biol. Bull. 194, 116–119 (1998).

    Article  CAS  PubMed  Google Scholar 

  139. Kubota, N., Kanemori, M., Sasayama, Y., Aida, M. & Fukumori, Y. Identification of endosymbionts in Oligobrachia mashikoi (Siboglinidae, Annelida). Microbes Environ. 22, 136–144 (2007).

    Article  Google Scholar 

  140. Thornhill, D. J. et al. Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida). Biol. Bull. 214, 135–144 (2008).

    Article  CAS  PubMed  Google Scholar 

  141. Goffredi, S. K., Jones, W. J., Erhlich, H., Springer, A. & Vrijenhoek, R. C. Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ. Microbiol. 28 June 2008 (doi: 10.1111/j.1462-2920.2008.01684.x).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Max Planck Society, the German Research Foundation (DFG) Cluster of Excellence at MARUM Bremen, and the DFG-Priority Program 1144: From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes (contribution number 28). We are grateful to the Census of Marine Life working group ChEss for its support of research on the biogeography of chemosynthetic ecosystems. We particularly thank the members of the Symbiosis Group of the Max Planck Institute Bremen for their enthusiasm about and discussions of chemosynthetic symbioses. We also thank the anonymous reviewers for helpful suggestions that improved this review. Much of the early literature on chemosynthetic symbioses is not cited here owing to space limitations.

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  1. Symbiosis Group, Max Planck Institute for Marine Microbiology, Celsiusstr. 1, Bremen, D-28359, Germany

    Nicole Dubilier & Claudia Bergin

  2. HYDRA Institute for Marine Sciences, Elba Field Station, Fetovaia, Via del Forno 80, Campo nell'Elba (LI), I-57034, Italy

    Christian Lott

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Glossary

Chemolithoautotrophic

Chemolithoautotrophic organisms use a chemical compound as an energy source, an inorganic compound, such as sulphide, as an electron donor and an inorganic carbon source (usually carbon dioxide) to synthesize organic carbon.

Phototrophic

Phototrophic organisms, such as plants, use light to gain energy.

Heterotrophic

Heterotrophic organisms, such as humans, use an organic source of carbon.

Chemoautotrophic

The term chemoautotrophic is often used as a synonym for chemolithoautotrophic. However, some chemoautotrophs use organic compounds as electron donors; these organisms are called chemoorganoautotrophs.

Chemosynthetic

Describes two types of organisms: chemolithoautotrophs (for example, sulphur oxidizers) and methane oxidizers. These organisms convert one or more carbon molecules (usually carbon dioxide or methane) into organic matter using the oxidation of inorganic compounds (for example, sulphide) or methane as a source of energy. Both symbiotic and free-living chemosynthetic microorganisms are primary producers; they form the basis of the food chain at vents and seeps.

Thiotrophic

An organism that uses reduced sulphur compounds, such as sulphide, as electron donors is called a thiotroph or sulphur oxidizer.

Meiofauna

Small free-living invertebrates that live in marine and fresh-water sediments. Meiofauna do not constitute a defined taxonomic rank but rather are a group of benthic animals that are defined by their size (in general, these organisms can pass through a 1 mm sieve, but are retained on a 0.45 μm sieve).

Epibiont

A symbiont that lives on the surface of its host.

Endobiont

A symbiont that lives inside its host.

Methanotrophic

An organism that uses methane as an energy and carbon source is called a methanotroph or methane oxidizer.

Syntrophy

Strictly defined, syntrophy describes a nutritional relationship between two organisms that combine their metabolic capabilities to use a substrate that neither could use alone. In this Review, we use syntrophy loosely to describe the beneficial exchange of products between two or more organisms.

Population bottleneck

An evolutionary event in which the size of a population is greatly reduced.

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Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6, 725–740 (2008). https://doi.org/10.1038/nrmicro1992

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