A Lytic Polysaccharide Monooxygenase from a White-Rot Fungus Drives the Degradation of Lignin by a Versatile Peroxidase.

Lytic polysaccharide monooxygenases (LPMOs), a class of copper-dependent enzymes, play a crucial role in boosting the enzymatic decomposition of polysaccharides. Here, we reveal that LPMOs might be associated with a lignin degradation pathway. An LPMO from white-rot fungus , LPMO9A (LPMO9A), was shown to be able to efficiently drive the activity of class II lignin-degrading peroxidases through HO production regardless of the presence or absence of a cellulose substrate. An LPMO-driven peroxidase reaction can degrade β-O-4 and 5-5' types of lignin dimer with 46.5% and 37.7% degradation, respectively, as well as alter the structure of natural lignin and kraft lignin. HO generated by LPMO9A was preferentially utilized for the peroxidase from sp. strain P18 (VP) reaction rather than cellulose oxidation, indicating that white-rot fungi may have a strategy for preferential degradation of resistant lignin. This discovery shows that LPMOs may be involved in lignin oxidation as auxiliary enzymes of lignin-degrading peroxidases during the white-rot fungal decay process. The enzymatic biodegradation of structural polysaccharides is affected by the degree of delignification of lignocellulose during the white-rot fungal decay process. The lignin matrix decreases accessibility to the substrates for LPMOs. HO has been studied as a cosubstrate for LPMOs, but the formation and utilization of HO in the reactions still represent an intriguing focus of current research. Lignin-degrading peroxidases and LPMOs usually coexist during fungal decay, and therefore, the relationship between HO-dependent lignin-degrading peroxidases and LPMOs should be considered during the wood decay process. The current study revealed that white-rot fungal LPMOs may be involved in the degradation of lignin through driving a versatile form of peroxidase activity and that HO generated by LPMO9A was preferentially used for lignin oxidation by lignin-degrading peroxidase (VP). These findings reveal a potential relationship between LPMOs and lignin degradation, which will be of great significance for further understanding the contribution of LPMOs to the white-rot fungal decay process.