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

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 monito...

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Autores principales: Shah, Firoz, Gressler, Markus, Nehzati, Susan, Op De Beeck, Michiel, Gentile, Luigi, Hoffmeister, Dirk, Persson, Per, Tunlid, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7824621/
https://www.ncbi.nlm.nih.gov/pubmed/33374225
http://dx.doi.org/10.3390/microorganisms9010035
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author Shah, Firoz
Gressler, Markus
Nehzati, Susan
Op De Beeck, Michiel
Gentile, Luigi
Hoffmeister, Dirk
Persson, Per
Tunlid, Anders
author_facet Shah, Firoz
Gressler, Markus
Nehzati, Susan
Op De Beeck, Michiel
Gentile, Luigi
Hoffmeister, Dirk
Persson, Per
Tunlid, Anders
author_sort Shah, Firoz
collection PubMed
description 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.
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spelling pubmed-78246212021-01-24 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 Microorganisms Article 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. MDPI 2020-12-24 /pmc/articles/PMC7824621/ /pubmed/33374225 http://dx.doi.org/10.3390/microorganisms9010035 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Shah, Firoz
Gressler, Markus
Nehzati, Susan
Op De Beeck, Michiel
Gentile, Luigi
Hoffmeister, Dirk
Persson, Per
Tunlid, Anders
Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title_full Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title_fullStr Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title_full_unstemmed Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title_short Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus Paxillus involutus
title_sort secretion of iron(iii)-reducing metabolites during protein acquisition by the ectomycorrhizal fungus paxillus involutus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7824621/
https://www.ncbi.nlm.nih.gov/pubmed/33374225
http://dx.doi.org/10.3390/microorganisms9010035
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