An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion

Federico Sabbadin,Giovanna Pesante,Katrin Beßer ,Sean T Sweeney,Theodora Tryfona,G.j Davies ,G.r Hemsworth ,Luisa Elias,Rita D Marques ,Luisa Ciano,Neil C Bruce,Rachel Bates,Paul H Walton,Paul Dupree,Yang Li ,Bernard Henrissat,Adam Dowle ,Rachael Simister,Leonardo D Gomez,Simon J Mcqueen‐Mason

doi:10.1038/s41467-018-03142-x

Abstract

Thermobia domestica belongs to an ancient group of insects and has a remarkable ability to digest crystalline cellulose without microbial assistance. By investigating the digestive proteome of Thermobia, we have identified over 20 members of an uncharacterized family of lytic polysaccharide monooxygenases (LPMOs). We show that this LPMO family spans across several clades of the Tree of Life, is of ancient origin, and was recruited by early arthropods with possible roles in remodeling endogenous chitin scaffolds during development and metamorphosis. Based on our in-depth characterization of Thermobia’s LPMOs, we propose that diversification of these enzymes toward cellulose digestion might have endowed ancestral insects with an effective biochemical apparatus for biomass degradation, allowing the early colonization of land during the Paleozoic Era. The vital role of LPMOs in modern agricultural pests and disease vectors offers new opportunities to help tackle global challenges in food security and the control of infectious diseases.

Highlights

Thermobia domestica belongs to an ancient group of insects and has a remarkable ability to digest crystalline cellulose without microbial assistance
High-performance anion-exchange chromatography (HPAEC) analysis of the fluids of the crop from animals grown on Avicel showed a dominant peak corresponding to glucose, indicating that crystalline cellulose had been broken down to its monomeric unit (Fig. 1e)
Our analysis revealed that the gut proteome of Thermobia is dominated by recognizable carbohydrate active enzymes (CAZymes, Fig. 1f, Supplementary Datas 1–4) that make up around half of the total protein content

Summary

Introduction

Thermobia domestica belongs to an ancient group of insects and has a remarkable ability to digest crystalline cellulose without microbial assistance. Known as the firebrat, Thermobia domestica (Fig. 1a) is a detritivorous insect related to the silverfish and belonging to the order of Zygentoma, one of the most primitive groups of insects that appeared on land during the Devonian Period (420 million years ago)[8] These animals can efficiently digest crystalline cellulose at rates comparable to cows and termites, but unlike these animals, digestion in firebrats is accomplished without microbial assistance, making the endogenous proteins responsible for biomass utilization of significant importance to both evolutionary entomology and industrial biotechnology[9,10,11,12,13]. In-depth biochemical, structural, and spectroscopic data, gene expression patterns, and gene suppression phenotypes suggest that these ancient LPMOs play crucial roles in arthropod development and food digestion, and represent a new range of tools to help tackle major challenges in agriculture and public health

Methods

Results

Conclusion