Involutin Is an Fe ³⁺ Reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-Based Decomposition of Organic Matter

Abstract

Ectomycorrhizal fungi play a key role in mobilizing nutrients embedded in recalcitrant organic matter complexes, thereby increasing nutrient accessibility to the host plant. Recent studies have shown that during the assimilation of nutrients, the ectomycorrhizal fungus Paxillus involutus decomposes organic matter using an oxidative mechanism involving Fenton chemistry (Fe2+ + H2O2 + H+ → Fe3+ + ˙OH + H2O), similar to that of brown rot wood-decaying fungi. In such fungi, secreted metabolites are one of the components that drive one-electron reductions of Fe3+ and O2, generating Fenton chemistry reagents. Here we investigated whether such a mechanism is also implemented by P. involutus during organic matter decomposition. Activity-guided purification was performed to isolate the Fe3+-reducing principle secreted by P. involutus during growth on a maize compost extract. The Fe3+-reducing activity correlated with the presence of one compound. Mass spectrometry and nuclear magnetic resonance (NMR) identified this compound as the diarylcyclopentenone involutin. A major part of the involutin produced by P. involutus during organic matter decomposition was secreted into the medium, and the metabolite was not detected when the fungus was grown on a mineral nutrient medium. We also demonstrated that in the presence of H2O2, involutin has the capacity to drive an in vitro Fenton reaction via Fe3+ reduction. Our results show that the mechanism for the reduction of Fe3+ and the generation of hydroxyl radicals via Fenton chemistry by ectomycorrhizal fungi during organic matter decomposition is similar to that employed by the evolutionarily related brown rot saprotrophs during wood decay.

Mineral surface‐reactive metabolites secreted during fungal decomposition contribute to the formation of soil organic matter

“…In these fungi, Fenton chemistry reagents are generated by the secreted metabolites, including hydroquinones and catechols, that drive one‐electron reductions of Fe 3+ and O 2 (Hatakka and Hammel, ). The major Fe 3+ ‐reducing metabolite produced by P. involutus during Fenton‐based OM decomposition is the diarylcyclopentenone involution (Shah et al ., ); recent studies have shown that genes encoding enzymes involved in the biosynthesis of this metabolite are expressed during DOM decomposition (Shah et al ., ). Another group of fungal metabolites with aromatic and/or phenolic structures are the polyketides (Keller et al ., ; Hertweck, ).…”

Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus

“…In brown rot fungi, secreted metabolites are produced by the fungus that drive one‐electron reduction of Fe 3+ and O 2 , generating the Fenton chemistry reagents Fe 2+ and H 2 O 2 (Hatakka & Hammel, ). One such Fe 3+ ‐reducing metabolite, the diarylcyclopentenone involutin, is also secreted by P. involutus during SOM decomposition (Shah et al ., ), but the source of H 2 O 2 in P. involutus remains unknown.…”

Biocatalytic portfolio of Basidiomycota

“…Two NRPS lacking the peptide-bond forming condensation domain have been biochemically characterized and shown to condense two aromatic α-keto acids to produce compounds with a quinone core as pigments or antimicrobials [63,65]. These secondary metabolites are also secreted as iron reductants to drive quinone redox cycling for lignin degradation [69]. Nevertheless, some intriguing PKS derived bioactive metabolites have been isolated from Basidiomycota.…”