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

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.

Lignocellulose degradation: An overview of fungi and fungal enzymes involved in lignocellulose degradation

“…LPMOs are copper-dependent enzymes that catalyze the oxidative cleavage of a glycosidic bond in the presence of hydrogen peroxide or dioxygen and an external electron donor [71]. They are able to degrade insoluble polysaccharides such as crystalline cellulose, chitin and starch [71][72][73][74]. Also, they depolymerise noncrystalline or soluble hemicellulosic substrates such as xyloglucan, xylan, and beta-glucans [75].…”

Detection and Characterization of a Novel Copper‐Dependent Intermediate in a Lytic Polysaccharide Monooxygenase

“…With the discovery of lytic polysaccharide monooxygenases (LPMOs), it was shown for the first time, how an enzyme with a single copper ion in the active site can activate dioxygen to break carbon–hydrogen bonds and degrade the most abundant and recalcitrant polysaccharides, such as cellulose and chitin . Since their discovery, LPMOs have been found in fungi, bacteria, virus, invertebrates, and algae, highlighting their biological importance . The diversity of identified LPMOs has increased with currently seven different families classified in the CAZY database as auxiliary activity (AA) AA9, AA10, AA11, AA13, AA14, AA15, and AA16 families .…”

Polysaccharide oxidation by lytic polysaccharide monooxygenase is enhanced by engineered cellobiose dehydrogenase

“…Lytic polysaccharide monooxygenases (LPMOs, EC: 1.14.99.53-56, CAZy IDs: AA9-11, AA13-16) are copper-containing enzymes found in chitin-, starch-, and plant cell wall-degrading organisms [1][2][3][4][5]. LPMOs use an unprecedented oxidative reaction mechanism to cleave and locally decrystallize these biopolymers, which enhances the activity of associated hydrolases [1,2,[6][7][8].…”