Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans

Katrin Beßer ,Samuel J Page,Neil C Bruce,Lourdes Cruz Garcia,Leonardo D Gomez,Giovanni Paro Da Cunha,Paul Dupree,Ray Dupree,Jefferson G Filgueiras,William Eborall ,Federico Sabbadin,Giovanna Pesante,Eduardo Ribeiro De Azevêdo ,Clare G Steele-King ,Igor Polikarpov,Marcelo Kern,Luisa Elias,Simon M Cragg,Shaza Eva Mohamad ,Yang Li ,Graham P Malyon,Adam Dowle,Simon J Mcqueen‐Mason

doi:10.1038/s41467-018-07575-2

Abstract

Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Marine crustacean woodborers of the genus Limnoria are among the few animals that can survive on a diet of this recalcitrant material without relying on gut resident microbiota. Analysis of fecal pellets revealed that Limnoria targets hexose-containing polysaccharides (mainly cellulose, and also glucomannans), corresponding with the abundance of cellulases in their digestive system, but xylans and lignin are largely unconsumed. We show that the limnoriid respiratory protein, hemocyanin, is abundant in the hindgut where wood is digested, that incubation of wood with hemocyanin markedly enhances its digestibility by cellulases, and that it modifies lignin. We propose that this activity of hemocyanins is instrumental to the ability of Limnoria to feed on wood in the absence of gut symbionts. These findings may hold potential for innovations in lignocellulose biorefining.

Highlights

Woody plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin
We carried out mass loss studies and compositional analyses comparing wood fed to Limnoria with their excreted fecal pellets (Fig. 1a) to gain insights into the lignocellulose digestion process
Most, if not all, of this mass loss is associated with digestion of the partially crystalline cellulose fraction, of which more than half was removed, whereas the typically more accessible hemicellulose fraction, as well as lignin, accumulate in the fecal pellets and show little change in relative amounts when normalized to mass loss (Fig. 1b)

Summary

Introduction

Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Lignocellulosic, woody tissues provide mechanical support to higher plants They are formed of a macromolecular composite of cellulose microfibrils coated and bound to one another by hemicellulose and lignin, producing a strong material that is resistant to biological and chemical degradation[1]. Cellulose is made of β-1,4-linked glucan polymers that form strong paracrystalline microfibrils, whereas the hemicellulose may be galactoglucomannans in softwoods (produced by gymnosperms such as pine) or predominantly glucuronoxylans in hardwoods (produced by angiosperms such as willow)[2] These polysaccharides typically comprise ~70% of the wood, but are rendered hard to access within a hydrophobic macromolecular material interpenetrated and bound by the polyphenolic lignin. Besides the well-studied capability of bacteria to degrade cellulose and hemicellulose, there is growing evidence of their ligninolytic capacity by the utilization of peroxidases, laccases, and superoxide dismutases[14,15]

Methods

Results

Conclusion