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

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 in which a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.

Observations on the Life History and Geographic Range of the Giant Chemosymbiotic Shipworm Kuphus polythalamius (Bivalvia: Teredinidae).

Kuphus polythalamius (Teredinidae) is one of the world's largest, most rarely observed, and least understood bivalves. Kuphus polythalamius is also among the few shallow-water marine species and the only teredinid species determined to harbor sulfur-oxidizing chemoautotrophic (thioautotrophic) symbionts. Until the recent discovery of living specimens in the Philippines, this species was known only from calcareous hard parts, fossils, and the preserved soft tissues of a single large specimen. As a result, the anatomy, biology, life history, and geographic range of K. polythalamius remain obscure. Here we report the collection and description of the smallest living specimens of K. polythalamius yet discovered and confirm the species identity of these individuals by using sequences of three genetic markers. Unlike previously collected specimens, all of which have been reported to occur in marine sediments, these specimens were observed burrowing in wood, the same substrate utilized by all other members of the family. These observations suggest that K. polythalamius initially settles on wood and subsequently transitions into sediment, where this species may grow to enormous sizes. This discovery led us to search for and find previously unidentified and misidentified wood-boring specimens of this species within museum collections, and it allowed us to show that the recent geographic range (since 1933) of this species extends across a 3000-mile span from the Philippines to Papua New Guinea and the Solomon Islands.