The white rot basidiomycete Gelatoporia subvermispora produces fatty aldehydes that enable fungal manganese peroxidases to degrade recalcitrant lignin structures

• Published in: Applied and environmental microbiology Vol. 90; no. 4; p. e0204423
• Main Authors: Kapich, Alexander N, Suzuki, Hideki, Hirth, Kolby C, Fernández-Fueyo, Elena, Martínez, Angel T, Houtman, Carl J, Hammel, Kenneth E
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 17-04-2024
• Subjects: Aldehydes; Basidiomycota - metabolism; Biodegradation; Catalase; Decay; Fatty Acids; Free radicals; Fungal Proteins - metabolism; Hardwoods; Hexanal; Lignin; Lignin - metabolism; Lipids; Low molecular weights; Manganese; Metabolites; Molecular weight; Mycology; Oxidants; Oxidation; Oxidizing agents; Peroxidases - metabolism; Peroxidation; Polyporales; Veratryl alcohol; White rot; White rot fungi; Wood; white rot fungus; fatty aldehydes; free radicals; ligninolysis; manganese peroxidase
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/aem.02044-23

The ability of some white rot basidiomycetes to remove lignin selectively from wood indicates that low molecular weight oxidants have a role in ligninolysis. These oxidants are likely free radicals generated by fungal peroxidases from compounds in the biodegrading wood. Past work supports a role for manganese peroxidases (MnPs) in the production of ligninolytic oxidants from fungal membrane lipids. However, the fatty acid alkylperoxyl radicals initially formed during this process are not reactive enough to attack the major structures in lignin. Here, we evaluate the hypothesis that the peroxidation of fatty aldehydes might provide a source of more reactive acylperoxyl radicals. We found that
produced
2-nonenal,
octenal, and n-hexanal (a likely metabolite of
2,4-decadienal) during the incipient decay of aspen wood. Fungal fatty aldehydes supported the
oxidation by MnPs of a nonphenolic lignin model dimer, and also of the monomeric model veratryl alcohol. Experiments with the latter compound showed that the reactions were partially inhibited by oxalate, the chelator that white rot fungi employ to detach Mn
from the MnP active site, but nevertheless proceeded at its physiological concentration of 1 mM. The addition of catalase was inhibitory, which suggests that the standard MnP catalytic cycle is involved in the oxidation of aldehydes. MnP oxidized
2-nonenal quantitatively to
2-nonenoic acid with the consumption of one O
equivalent. The data suggest that when Mn
remains associated with MnP, it can oxidize aldehydes to their acyl radicals, and the latter subsequently add O
to become ligninolytic acylperoxyl radicals.IMPORTANCEThe biodegradation of lignin by white rot fungi is essential for the natural recycling of plant biomass and has useful applications in lignocellulose bioprocessing. Although fungal peroxidases have a key role in ligninolysis, past work indicates that biodegradation is initiated by smaller, as yet unidentified oxidants that can infiltrate the substrate. Here, we present evidence that the peroxidase-catalyzed oxidation of naturally occurring fungal aldehydes may provide a source of ligninolytic free radical oxidants.