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

Federico Sabbadin (1) , Glyn Hemsworth (2) , Luisa Ciano (1) , Bernard Henrissat (3) , Paul P. Dupree (4) , Theodora T. Tryfona (4) , Rita Marques (4) , Sean Sweeney (1) , Katrin Besser (1) , Luisa Elias (1) , Giovanna Pesante (1) , Yi Li (1) , Adam Dowle (1) , Rachel Bates (1) , Leonardo Gomez (1) , Rachael Simister (1) , Gideon Davies (1) , Paul Walton (1) , Neil D.B. Bruce (1) , Simon Mcqueen-Mason (1)

1 University of York [York, UK]
2 University of Leeds
3 AFMB - Architecture et fonction des macromolécules biologiques
4 CAM - University of Cambridge [UK]

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.

Keywords: Polysaccharides; Proteomics; Phylogeny; Enzymes

Domains: Life Sciences [q-bio]; Biochemistry, Molecular Biology; Biochemistry [q-bio.BM]

Federico Sabbadin, Glyn Hemsworth, Luisa Ciano, Bernard Henrissat, Paul P. Dupree, et al.. An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nature Communications, 2018, 9 (1), pp.756. ⟨10.1038/s41467-018-03142-x⟩. ⟨hal-02094604⟩