Efficient lignin depolymerization is unique to the wood decay basidiomycetes, collectively referred to as white rot fungi.
Phanerochaete chrysosporium
simultaneously degrades lignin and cellulose, whereas the closely related species,
Ceriporiopsis subvermispora,
also depolymerizes lignin but may do so with relatively little cellulose degradation. To investigate the basis for selective ligninolysis, we conducted comparative genome analysis of
C. subvermispora
and
P. chrysosporium
. Genes encoding manganese peroxidase numbered 13 and five in
C. subvermispora
and
P. chrysosporium
, respectively. In addition, the
C. subvermispora
genome contains at least seven genes predicted to encode laccases, whereas the
P. chrysosporium
genome contains none. We also observed expansion of the number of
C. subvermispora
desaturase-encoding genes putatively involved in lipid metabolism. Microarray-based transcriptome analysis showed substantial up-regulation of several desaturase and MnP genes in wood-containing medium. MS identified MnP proteins in
C. subvermispora
culture filtrates, but none in
P. chrysosporium
cultures. These results support the importance of MnP and a lignin degradation mechanism whereby cleavage of the dominant nonphenolic structures is mediated by lipid peroxidation products. Two
C. subvermispora
genes were predicted to encode peroxidases structurally similar to
P. chrysosporium
lignin peroxidase and, following heterologous expression in
Escherichia coli
, the enzymes were shown to oxidize high redox potential substrates, but not Mn
2+
. Apart from oxidative lignin degradation, we also examined cellulolytic and hemicellulolytic systems in both fungi. In summary, the
C. subvermispora
genetic inventory and expression patterns exhibit increased oxidoreductase potential and diminished cellulolytic capability relative to
P. chrysosporium
.
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.
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