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

Abstract

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 Pleurotus ostreatus, LPMO9A (PoLPMO9A), was shown to be able to efficiently drive the activity of class II lignin-degrading peroxidases in vitro through H2O2 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. H2O2 generated by PoLPMO9A was preferentially utilized for the peroxidase from Physisporinus sp. strain P18 (PsVP) 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. IMPORTANCE 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. H2O2 has been studied as a cosubstrate for LPMOs, but the formation and utilization of H2O2 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 H2O2-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 in vitro and that H2O2 generated by PoLPMO9A was preferentially used for lignin oxidation by lignin-degrading peroxidase (PsVP). 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.

Fungal Treatment for the Valorization of Technical Soda Lignin

“…Electron donors include lignin-derived compounds released during biodegradation, diphenols produced by the reaction of different AA3, and by cellobiose dehydrogenases (AA8) [ 65 ]. A recent study has shown that H 2 O 2 generated by LPMO was favorably used for lignin oxidation by the lignin-degrading peroxidases rather than for cellulose oxidation [ 66 ]. The induction of LPMO and their coupled secretion with AA3_1 support their role in lignin modification.…”

Enzymatic processing of lignocellulosic biomass: principles, recent advances and perspectives

“…Importantly, lignin-active enzymes can affect the electrondonating and H 2 O 2 -generating abilities of lignin, providing possible links between polysaccharide-and lignin-degrading enzyme systems [42,115,269]. Another possible link between these systems is that LPMO-facilitated in situ production of H 2 O 2 may be utilized by peroxidases to degrade lignin [213].…”

Kinetic insights into the peroxygenase activity of cellulose-active lytic polysaccharide monooxygenases (LPMOs)

“…The auto oxidation of reductants by O 2 often leads to the formation of H 2 O 2 and this complicates the interpretation of kinetic data. Furthermore, LPMOs that are free from substrate have both reductant oxidase 23 and peroxidase 16,18 activity where the oxidase activity leads to the formation of H 2 O 2 17,[23][24][25] .…”