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Involutin is a Fe3+ reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-based Decomposition of Organic Matter.

Shah, Firoz LU ; Schwenk, Daniel; Cuevas, César Nicolás LU ; Persson, Per LU ; Hoffmeister, Dirk and Tunlid, Anders LU (2015) In Applied and Environmental Microbiology 81(24). p.8427-8433
Abstract
Ectomycorrhizal fungi play a key role in mobilizing nutrients embedded in recalcitrant organic matter complexes, thereby increasing nutrient accessibility to the host plant. Recent study have shown that during assimilation of nutrients, the ectomycorrhizal fungus Paxillus involutus decomposes organic matter using an oxidative mechanism involving Fenton chemistry (Fe(2+) + H2O2 + H(+) → Fe(3+) + •OH + H2O) similar to that of brown-rot wood-decaying fungi. In such fungi, secreted metabolites are one of the components that drive one-electron reductions of Fe(3+) and O2, generating Fenton chemistry reagents. Here, we investigated whether such a mechanism is also implemented by P. involutus during organic matter decomposition. Activity-guided... (More)
Ectomycorrhizal fungi play a key role in mobilizing nutrients embedded in recalcitrant organic matter complexes, thereby increasing nutrient accessibility to the host plant. Recent study have shown that during assimilation of nutrients, the ectomycorrhizal fungus Paxillus involutus decomposes organic matter using an oxidative mechanism involving Fenton chemistry (Fe(2+) + H2O2 + H(+) → Fe(3+) + •OH + H2O) similar to that of brown-rot wood-decaying fungi. In such fungi, secreted metabolites are one of the components that drive one-electron reductions of Fe(3+) and O2, generating Fenton chemistry reagents. Here, we investigated whether such a mechanism is also implemented by P. involutus during organic matter decomposition. Activity-guided purification was performed to isolate the Fe(3+)-reducing principle secreted by P. involutus during growth on maize compost extract. The Fe(3+)-reducing activity correlated with the presence of one compound. Mass spectrometry and NMR identified this compound as the diarylcyclopentenone involutin. A major part of the involutin produced by P. involutus during organic matter decomposition was secreted into the medium and the metabolite was not detected when the fungus was grown on a mineral nutrient medium. We also demonstrated that in the presence of H2O2, involutin has the capacity to drive an in vitro Fenton reaction via Fe(3+) reduction. Our results show that the mechanism for reducing Fe(3+) and generating hydroxyl radicals via Fenton chemistry by ectomycorrhizal fungi during organic matter decomposition is similar to that expressed by the evolutionarily related brown-rot saprotrophs during wood decay. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Applied and Environmental Microbiology
volume
81
issue
24
pages
8427 - 8433
publisher
American Society for Microbiology
external identifiers
  • pmid:26431968
  • wos:000365212800017
  • scopus:84949657782
ISSN
0099-2240
DOI
10.1128/AEM.02312-15
project
MICCS - Molecular Interactions Controlling soil Carbon Sequestration
language
English
LU publication?
yes
id
10927826-53b9-43a1-8bab-048dd7d909b4 (old id 8159027)
date added to LUP
2015-11-12 13:37:58
date last changed
2017-06-25 03:04:08
@article{10927826-53b9-43a1-8bab-048dd7d909b4,
  abstract     = {Ectomycorrhizal fungi play a key role in mobilizing nutrients embedded in recalcitrant organic matter complexes, thereby increasing nutrient accessibility to the host plant. Recent study have shown that during assimilation of nutrients, the ectomycorrhizal fungus Paxillus involutus decomposes organic matter using an oxidative mechanism involving Fenton chemistry (Fe(2+) + H2O2 + H(+) → Fe(3+) + •OH + H2O) similar to that of brown-rot wood-decaying fungi. In such fungi, secreted metabolites are one of the components that drive one-electron reductions of Fe(3+) and O2, generating Fenton chemistry reagents. Here, we investigated whether such a mechanism is also implemented by P. involutus during organic matter decomposition. Activity-guided purification was performed to isolate the Fe(3+)-reducing principle secreted by P. involutus during growth on maize compost extract. The Fe(3+)-reducing activity correlated with the presence of one compound. Mass spectrometry and NMR identified this compound as the diarylcyclopentenone involutin. A major part of the involutin produced by P. involutus during organic matter decomposition was secreted into the medium and the metabolite was not detected when the fungus was grown on a mineral nutrient medium. We also demonstrated that in the presence of H2O2, involutin has the capacity to drive an in vitro Fenton reaction via Fe(3+) reduction. Our results show that the mechanism for reducing Fe(3+) and generating hydroxyl radicals via Fenton chemistry by ectomycorrhizal fungi during organic matter decomposition is similar to that expressed by the evolutionarily related brown-rot saprotrophs during wood decay.},
  author       = {Shah, Firoz and Schwenk, Daniel and Cuevas, César Nicolás and Persson, Per and Hoffmeister, Dirk and Tunlid, Anders},
  issn         = {0099-2240},
  language     = {eng},
  number       = {24},
  pages        = {8427--8433},
  publisher    = {American Society for Microbiology},
  series       = {Applied and Environmental Microbiology},
  title        = {Involutin is a Fe3+ reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-based Decomposition of Organic Matter.},
  url          = {http://dx.doi.org/10.1128/AEM.02312-15},
  volume       = {81},
  year         = {2015},
}