Uncovering the molecular mechanisms of lignocellulose digestion in shipworms

Federico Sabbadin,Neil C Bruce,Deborah A Rathbone,Adam A Dowle,Katrin Besser,Simon M Cragg,Simon J Mcqueen-Mason,J Reuben Shipway,Meg Stark,Rachel Bates,Giovanna Pesante,Luisa Elias,Yi Li,Clare Steele-King

doi:10.1186/s13068-018-1058-3

Federico Sabbadin, Neil C Bruce + Show 12 more

Open Access

https://doi.org/10.1186/s13068-018-1058-3

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Abstract

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.

Highlights

Large amounts of wood from terrestrial plants enter the marine environment and support complex ecosystems
While compelling evidence has shown that gill bacteriocytes are the main site for the production of bacterial carbohydrate active enzymes (CAZymes) in shipworms, several authors have hypothesized that the digestive gland might be responsible for the synthesis of endogenous enzymes, while the cecum appears to be the site of wood breakdown and could potentially be involved in sugar uptake [2, 4]
In order to identify the key genes involved in wood digestion and absorption of breakdown products in L. pedicellatus, we performed meta-transcriptome sequencing from the main organs putatively involved in wood digestion (Fig. 1a, Additional file 1: Table S1) using healthy adult L. pedicellatus growing in blocks of Scots pine submerged in sea water

Summary

Introduction

Large amounts of wood from terrestrial plants enter the marine environment and support complex ecosystems. It has been shown that around 70% of dead wood in mangroves is processed by the action of wood-boring bivalve molluscs known as shipworms [2, 3]. Shipworms acquired their name due to their devastating effects on wooden ships prior to the advent of copper-bottoming, a process. Shipworms burrow cylindrical tunnels using specialized shell valves with abrasive toothed ridges as a rasp and ingest the wood particles as they burrow.

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