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Research article2021Peer reviewedOpen access

Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus

Shah, Firoz; Gressler, Markus; Nehzati, Susan; Op De Beeck, Michiel; Gentile, Luigi; Hoffmeister, Dirk; Persson, Per; Tunlid, Anders

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 (center dot 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 center dot 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.

Keywords

ectomycorrhizal fungi; Fenton reaction; involutin; iron reduction; secondary metabolites

Published in

Microorganisms
2021, Volume: 9, number: 1, article number: 35

    UKÄ Subject classification

    Microbiology

    Publication identifier

    DOI: https://doi.org/10.3390/microorganisms9010035

    Permanent link to this page (URI)

    https://res.slu.se/id/publ/109795