Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory

Daniel L. Distel, Marvin A. Altamia, Zhenjian Lin, J. Reuben Shipway, Andrew Han, Imelda Forteza, Rowena Antemano, Ma Gwen J.Peñaflor Limbaco, Alison G. Teboe, Rande Dechavez, Julie Albano, Gary Rosenberg, Gisela P. Concepcion, Eric W. Schmidt, Margo Haygood

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The "wooden-steps" hypothesis [Distel DL, et al. (2000) Nature 403:725-726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalve Kuphus polythalamia. This rare and enigmatic species,which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show that K. polythalamia harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate that K. polythalamia is a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example inwhich a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.

Original languageEnglish (US)
Pages (from-to)E3652-E3658
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number18
DOIs
StatePublished - May 2 2017
Externally publishedYes

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Symbiosis
Bivalvia
Hydrothermal Vents
Geologic Sediments
Digestive System
Hydrogen Sulfide
Sulfur
Ecosystem
Digestion
Bacteria
Food

Keywords

  • Chemoautotrophy
  • Shipworm
  • Symbiosis
  • Teredinidae
  • Thioautotrophy

ASJC Scopus subject areas

  • General

Cite this

Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia : Teredinidae) extends wooden-steps theory. / Distel, Daniel L.; Altamia, Marvin A.; Lin, Zhenjian; Shipway, J. Reuben; Han, Andrew; Forteza, Imelda; Antemano, Rowena; Limbaco, Ma Gwen J.Peñaflor; Teboe, Alison G.; Dechavez, Rande; Albano, Julie; Rosenberg, Gary; Concepcion, Gisela P.; Schmidt, Eric W.; Haygood, Margo.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 18, 02.05.2017, p. E3652-E3658.

Research output: Contribution to journalArticle

Distel, DL, Altamia, MA, Lin, Z, Shipway, JR, Han, A, Forteza, I, Antemano, R, Limbaco, MGJP, Teboe, AG, Dechavez, R, Albano, J, Rosenberg, G, Concepcion, GP, Schmidt, EW & Haygood, M 2017, 'Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 18, pp. E3652-E3658. https://doi.org/10.1073/pnas.1620470114
Distel, Daniel L. ; Altamia, Marvin A. ; Lin, Zhenjian ; Shipway, J. Reuben ; Han, Andrew ; Forteza, Imelda ; Antemano, Rowena ; Limbaco, Ma Gwen J.Peñaflor ; Teboe, Alison G. ; Dechavez, Rande ; Albano, Julie ; Rosenberg, Gary ; Concepcion, Gisela P. ; Schmidt, Eric W. ; Haygood, Margo. / Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia : Teredinidae) extends wooden-steps theory. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 18. pp. E3652-E3658.
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