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

Abstract

The "wooden-steps" hypothesis [Distel DL, et al. (2000) 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 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 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 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.

Secondary metabolism in the gill microbiota of shipworms (Teredinidae) as revealed by comparison of metagenomes and nearly complete symbiont genomes

“…Underlying this simplicity, for each bacterial species present in a sample, there are multiple strain variants. We measured the prevalence of these variants using a previously reported method in which we look at single nucleotide polymorphisms in conserved genes such as DNA gyrase B at the individual read level ( Figure S2) (7). The results are very similar to our previous report of bacterial strain variation in the gill metagenomes of K. polythalamius.…”

“…The gill metagenomes of two specimens of mud-dwelling K. polythalamius from Mindanao were previously sequenced (7). Here, we sequenced and analyzed gill metagenomes from a third wood-burrowing Kuphus sp.…”

“…The symbiont mixtures are representative of the animal lifestyles. K. polythalamius appears to thrive entirely on sulfide oxidation (7), as required in its sediment habitat, while the other shipworms contain various cellulolytic bacteria responsible for wood degradation. D. mannii likely has a more complex lifestyle, since it contains the sulfur-oxidizing bacterium strain 2719K and the cellulolytic species T. turnerae and strain 2753L.…”

“…Many shipworms eat wood, assisted by cellulases from intracellular symbiotic γproteobacteria that inhabit their gills (Figure 1) (3)(4)(5)(6). Others use sulfide metabolism also relying on gill-dwelling γ-proteobacteria for sulfur oxidation (7). Shipworm gill symbionts of several different species are thus essential to shipworm nutrition and survival.…”

“…Several shipworm species, such as Kuphus polythalamius, live in other substrates. K. polythalamius often is found in sediment habitats (as well as in wood) where its gill symbionts are crucial to sulfide oxidation and carry out carbon fixation (7). K. polythalamius lacks significant amounts of cellulolytic symbionts such as T. turnerae, and instead contains Thiosocius teredinicola, which oxidizes sulfide and generates energy for the host (21).…”