Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i>
The ectomycorrhizal fungus <i>Paxillus involutus</i> 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(I...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2020-12-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/9/1/35 |
| _version_ | 1797543638234824704 |
|---|---|
| author | Firoz Shah Markus Gressler Susan Nehzati Michiel Op De Beeck Luigi Gentile Dirk Hoffmeister Per Persson Anders Tunlid |
| author_facet | Firoz Shah Markus Gressler Susan Nehzati Michiel Op De Beeck Luigi Gentile Dirk Hoffmeister Per Persson Anders Tunlid |
| author_sort | Firoz Shah |
| collection | DOAJ |
| description | The ectomycorrhizal fungus <i>Paxillus involutus</i> 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 <i>P. involutus</i>. 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. |
| first_indexed | 2024-03-10T13:48:28Z |
| format | Article |
| id | doaj.art-75aeab1ce10d4ecfb79ce0608ccb5a5f |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T13:48:28Z |
| publishDate | 2020-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-75aeab1ce10d4ecfb79ce0608ccb5a5f2023-11-21T02:23:32ZengMDPI AGMicroorganisms2076-26072020-12-01913510.3390/microorganisms9010035Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i>Firoz Shah0Markus Gressler1Susan Nehzati2Michiel Op De Beeck3Luigi Gentile4Dirk Hoffmeister5Per Persson6Anders Tunlid7Microbial Ecology Group, Department of Biology, Lund University, 223 62 Lund, SwedenDepartment of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, 07747 Jena, GermanyMicrobial Ecology Group, Department of Biology, Lund University, 223 62 Lund, SwedenMicrobial Ecology Group, Department of Biology, Lund University, 223 62 Lund, SwedenMicrobial Ecology Group, Department of Biology, Lund University, 223 62 Lund, SwedenDepartment of Pharmaceutical Microbiology at the Hans Knöll Institute, Friedrich-Schiller-Universität, 07747 Jena, GermanyCentre for Environmental and Climate Research (CEC), Lund University, 223 62 Lund, SwedenMicrobial Ecology Group, Department of Biology, Lund University, 223 62 Lund, SwedenThe ectomycorrhizal fungus <i>Paxillus involutus</i> 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 <i>P. involutus</i>. 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.https://www.mdpi.com/2076-2607/9/1/35ectomycorrhizal fungiFenton reactioninvolutiniron reductionsecondary metabolites |
| spellingShingle | Firoz Shah Markus Gressler Susan Nehzati Michiel Op De Beeck Luigi Gentile Dirk Hoffmeister Per Persson Anders Tunlid Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> Microorganisms ectomycorrhizal fungi Fenton reaction involutin iron reduction secondary metabolites |
| title | Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> |
| title_full | Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> |
| title_fullStr | Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> |
| title_full_unstemmed | Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> |
| title_short | Secretion of Iron(III)-Reducing Metabolites during Protein Acquisition by the Ectomycorrhizal Fungus <i>Paxillus involutus</i> |
| title_sort | secretion of iron iii reducing metabolites during protein acquisition by the ectomycorrhizal fungus i paxillus involutus i |
| topic | ectomycorrhizal fungi Fenton reaction involutin iron reduction secondary metabolites |
| url | https://www.mdpi.com/2076-2607/9/1/35 |
| work_keys_str_mv | AT firozshah secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT markusgressler secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT susannehzati secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT michielopdebeeck secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT luigigentile secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT dirkhoffmeister secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT perpersson secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi AT anderstunlid secretionofironiiireducingmetabolitesduringproteinacquisitionbytheectomycorrhizalfungusipaxillusinvolutusi |