Abstract
The ectomycorrhizal fungus Paxillus involutus decomposes proteins using a two-step mechanism, including oxidation and proteolysis. Oxidation involves the action of extracellular hydroxyl radicals (•OH) generated by the Fenton reaction. This reaction requires the presence of iron(II). Here, we monitored the speciation of extracellular iron and the secretion of iron(III)-reducing metabolites during the decomposition of proteins by P. involutus. X-ray absorption spectroscopy showed that extracellular iron was mainly present as solid iron(III) phosphates and oxides. Within 1 to 2 days, these compounds were reductively dissolved, and iron(II) complexes were formed, which remained in the medium throughout the incubation. HPLC and mass spectrometry detected five extracellular iron(III)-reducing metabolites. Four of them were also secreted when the fungus grew on a medium containing ammonium as the sole nitrogen source. NMR identified the unique iron(III)-reductant as the diarylcyclopentenone involutin. Involutin was produced from day 2, just before the elevated •OH production, preceding the oxidation of BSA. The other, not yet fully characterized iron(III)-reductants likely participate in the rapid reduction and dissolution of solid iron(III) complexes observed on day one. The production of these metabolites is induced by other environmental cues than for involutin, suggesting that they play a role beyond the Fenton chemistry associated with protein oxidation.
Highlights
Introduction in published maps and institutionalA large part of the nitrogen (N) present in forest soils is found in organic forms, primarily as proteins and peptides
Enhanced OH production was observed from day 3 of the incubation period, which coincides with the depletion of ammonium in the growth medium [18]
48spectra h afterand starting the of incubation, be seen in the change of shape in the Thespectra first-derivative of X-ray near-edgecollected structureafter (XANES)
Summary
A large part of the nitrogen (N) present in forest soils is found in organic forms, primarily as proteins and peptides. These molecules are typically complexed with polyphenols, polysaccharides, lignin residues, and other degradation products of litter material that constitute soil organic matter (SOM) [1,2]. Organic and mineral N-containing complexes need to be decomposed by microorganisms before they become available to plants [5]. Considering the fact that ECM fungi have lost many of the genes encoding plant litter degrading enzymes that are present in saprotrophic fungi [7,8], the affiliations
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