No 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.

Lignocellulose forms the structural framework of woody plant biomass and represents the most abundant carbon source in the biosphere. Turnover of woody biomass is a critical component of the global carbon cycle, and the enzymes involved are of increasing industrial importance as industry moves away from fossil fuels to renewable carbon resources. Shipworms are marine bivalve molluscs that digest wood and play a key role in global carbon cycling by processing plant biomass in the oceans. Previous studies suggest that wood digestion in shipworms is dominated by enzymes produced by endosymbiotic bacteria found in the animal’s gills, while little is known about the identity and function of endogenous enzymes produced by shipworms. Using a combination of meta-transcriptomic, proteomic, imaging and biochemical analyses, we reveal a complex digestive system dominated by uncharacterized enzymes that are secreted by a specialized digestive gland and that accumulate in the cecum, where wood digestion occurs. Using a combination of transcriptomics, proteomics, and microscopy, we show that the digestive proteome of the shipworm Lyrodus pedicellatus is mostly composed of enzymes produced by the animal itself, with a small but significant contribution from symbiotic bacteria. The digestive proteome is dominated by a novel 300 kDa multi-domain glycoside hydrolase that functions in the hydrolysis of β-1,4-glucans, the most abundant polymers in wood. These studies allow an unprecedented level of insight into an unusual and ecologically important process for wood recycling in the marine environment, and open up new biotechnological opportunities in the mobilization of sugars from lignocellulosic biomass.Electronic supplementary materialThe online version of this article (10.1186/s13068-018-1058-3) contains supplementary material, which is available to authorized users.

Marine wood-boring teredinids, some of the most destructive wood borers in the sea, are a particularly difficult group to identify from morphological features. While in most bivalve species shell features are used as diagnostic characters, in the teredinids shell morphology shows high intraspecific variation and thus identification is based almost entirely on the morphology of the pallets. In the present study we aimed at improving ‘taxonomic resolution’ in teredinids by combining morphological evidence with mitochondrial and nuclear DNA sequences, respectively Cytochromec oxidase subunitI and small subunit rRNA 18S gene, to generate more rigorous and accessible identifications. DNA barcodes of Atlantic and Mediterranean populations of Lyrodus pedicellatus diverged by ~20%, suggesting cryptic species in the morphospecies L. pedicellatus. The low intraspecific divergence found in barcodes of specimens of Nototeredo norvagica (0.78%) confirms that Atlantic and Mediterranean forms of N. norvagica, the latter sometimes reported as Teredo utriculus, are the same species. Teredothyra dominicensis was found for the first time in the Mediterranean. A match was obtained between our 18S sequences and sequences of T. dominicensis from Netherlands Antilles, confirming that T. dominicensis in the Mediterranean is the same species that occurs in the Caribbean. There were differences in 18S sequences between Bankia carinata from the Mediterranean and Caribbean, which may indicate cryptic species.