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Secretion of iron(III)-reducing metabolites during protein acquisition by the ectomycorrhizal fungus paxillus involutus

Shah, Firoz LU ; Gressler, Markus ; Nehzati, Susan LU ; De Beeck, Michiel Op LU orcid ; Gentile, Luigi LU ; Hoffmeister, Dirk ; Persson, Per LU and Tunlid, Anders LU (2021) In Microorganisms 9(1).
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... (More)

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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; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Ectomycorrhizal fungi, Fenton reaction, Involutin, Iron reduction, Secondary metabolites
in
Microorganisms
volume
9
issue
1
article number
35
pages
16 pages
publisher
MDPI AG
external identifiers
  • pmid:33374225
  • scopus:85098768228
ISSN
2076-2607
DOI
10.3390/microorganisms9010035
language
English
LU publication?
yes
id
1065e120-f4f0-4bea-ab6b-8632b80446da
date added to LUP
2021-01-13 12:09:10
date last changed
2025-01-24 04:22:38
@article{1065e120-f4f0-4bea-ab6b-8632b80446da,
  abstract     = {{<p>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.</p>}},
  author       = {{Shah, Firoz and Gressler, Markus and Nehzati, Susan and De Beeck, Michiel Op and Gentile, Luigi and Hoffmeister, Dirk and Persson, Per and Tunlid, Anders}},
  issn         = {{2076-2607}},
  keywords     = {{Ectomycorrhizal fungi; Fenton reaction; Involutin; Iron reduction; Secondary metabolites}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{MDPI AG}},
  series       = {{Microorganisms}},
  title        = {{Secretion of iron(III)-reducing metabolites during protein acquisition by the ectomycorrhizal fungus paxillus involutus}},
  url          = {{http://dx.doi.org/10.3390/microorganisms9010035}},
  doi          = {{10.3390/microorganisms9010035}},
  volume       = {{9}},
  year         = {{2021}},
}