Uncovering the molecular mechanisms of lignocellulose digestion in shipworms

Lignocellulose forms the structural framework of woody plant biomass and represents the most abundant carbon source on the Planet. Turnover of woody biomass is a critical component of the planetary carbon cycle, and the enzymes involved are of increasing industrial importance as industry moves away from fossil to renewable carbon resources. Shipworms are marine bivalve molluscs that digest wood and play a key role in global carbon recycling by reprocessing 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 pedicellatusis mostly comprised 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 accounts for more than half of the total protein content in the cecum and 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.