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The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry.

Rineau, Francois LU ; Roth, Doris; Shah, Firoz LU ; Smits, Mark LU ; Johansson, Tomas LU ; Canbäck, Björn LU ; Olsen, Peter Bjarke; Persson, Per LU ; Grell, Morten Nedergaard and Lindquist, Erika, et al. (2012) In Environmental Microbiology 14(6). p.1477-1487
Abstract
Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter-protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded... (More)
Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter-protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown-rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown-rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical-based biodegradation system that can efficiently disrupt the organic matter-protein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems. (Less)
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organization
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Contribution to journal
publication status
published
subject
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Environmental Microbiology
volume
14
issue
6
pages
1477 - 1487
publisher
Wiley-Blackwell
external identifiers
  • wos:000304866600011
  • pmid:22469289
  • scopus:84861945371
ISSN
1462-2920
DOI
10.1111/j.1462-2920.2012.02736.x
project
BECC
Genome ecology of ectomycorrhizal fungi
language
English
LU publication?
yes
id
4d536a67-c7e6-4db5-90ca-576eb7a23c51 (old id 2519930)
date added to LUP
2012-05-08 11:46:09
date last changed
2017-11-12 03:17:31
@article{4d536a67-c7e6-4db5-90ca-576eb7a23c51,
  abstract     = {Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter-protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown-rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown-rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical-based biodegradation system that can efficiently disrupt the organic matter-protein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems.},
  author       = {Rineau, Francois and Roth, Doris and Shah, Firoz and Smits, Mark and Johansson, Tomas and Canbäck, Björn and Olsen, Peter Bjarke and Persson, Per and Grell, Morten Nedergaard and Lindquist, Erika and Grigoriev, Igor V and Lange, Lene and Tunlid, Anders},
  issn         = {1462-2920},
  language     = {eng},
  number       = {6},
  pages        = {1477--1487},
  publisher    = {Wiley-Blackwell},
  series       = {Environmental Microbiology},
  title        = {The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry.},
  url          = {http://dx.doi.org/10.1111/j.1462-2920.2012.02736.x},
  volume       = {14},
  year         = {2012},
}