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Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus

Op De Beeck, Michiel LU orcid ; Troein, Carl LU orcid ; Peterson, Carsten LU ; Persson, Per LU and Tunlid, Anders LU (2018) In New Phytologist 218(1). p.335-343
Abstract

Boreal trees rely on their ectomycorrhizal fungal symbionts to acquire growth-limiting nutrients, such as nitrogen (N), which mainly occurs as proteins complexed in soil organic matter (SOM). The mechanisms for liberating this N are unclear as ectomycorrhizal fungi have lost many genes encoding lignocellulose-degrading enzymes present in their saprotrophic ancestors. We hypothesized that hydroxyl radicals (bullOH), produced by the ectomycorrhizal fungus Paxillus involutus during growth on SOM, are involved in liberating organic N. Paxillus involutus was grown for 7 d on N-containing or N-free substrates that represent major organic compounds of SOM. bullOH production, ammonium assimilation, and proteolytic activity... (More)

Boreal trees rely on their ectomycorrhizal fungal symbionts to acquire growth-limiting nutrients, such as nitrogen (N), which mainly occurs as proteins complexed in soil organic matter (SOM). The mechanisms for liberating this N are unclear as ectomycorrhizal fungi have lost many genes encoding lignocellulose-degrading enzymes present in their saprotrophic ancestors. We hypothesized that hydroxyl radicals (bullOH), produced by the ectomycorrhizal fungus Paxillus involutus during growth on SOM, are involved in liberating organic N. Paxillus involutus was grown for 7 d on N-containing or N-free substrates that represent major organic compounds of SOM. bullOH production, ammonium assimilation, and proteolytic activity were measured daily. bullOH production was strongly induced when P. involutus switched from ammonium to protein as the main N source. Extracellular proteolytic activity was initiated shortly after the oxidation. Oxidized protein substrates induced higher proteolytic activity than unmodified proteins. Dynamic modeling predicted that bullOH production occurs in a burst, regulated mainly by ammonium and ferric iron concentrations. We propose that the production of bullOH and extracellular proteolytic enzymes are regulated by similar nutritional signals. Oxidation works in concert with proteolysis, improving N liberation from proteins in SOM. Organic N mining by ectomycorrhizal fungi has, until now, only been attributed to proteolysis.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Fenton reaction, Nitrogen (N), Paxillus involutus, Proteolysis, Soil organic matter (SOM)
in
New Phytologist
volume
218
issue
1
pages
335 - 343
publisher
Wiley-Blackwell
external identifiers
  • pmid:29297591
  • scopus:85039988426
ISSN
0028-646X
DOI
10.1111/nph.14971
project
MICCS - Molecular Interactions Controlling soil Carbon Sequestration
language
English
LU publication?
yes
id
4a9fdeeb-5b3b-427d-8ffd-5dfcbddd824b
date added to LUP
2018-01-15 08:47:11
date last changed
2024-04-15 01:20:22
@article{4a9fdeeb-5b3b-427d-8ffd-5dfcbddd824b,
  abstract     = {{<p>Boreal trees rely on their ectomycorrhizal fungal symbionts to acquire growth-limiting nutrients, such as nitrogen (N), which mainly occurs as proteins complexed in soil organic matter (SOM). The mechanisms for liberating this N are unclear as ectomycorrhizal fungi have lost many genes encoding lignocellulose-degrading enzymes present in their saprotrophic ancestors. We hypothesized that hydroxyl radicals (<sup>bull</sup>OH), produced by the ectomycorrhizal fungus Paxillus involutus during growth on SOM, are involved in liberating organic N. Paxillus involutus was grown for 7 d on N-containing or N-free substrates that represent major organic compounds of SOM. <sup>bull</sup>OH production, ammonium assimilation, and proteolytic activity were measured daily. <sup>bull</sup>OH production was strongly induced when P. involutus switched from ammonium to protein as the main N source. Extracellular proteolytic activity was initiated shortly after the oxidation. Oxidized protein substrates induced higher proteolytic activity than unmodified proteins. Dynamic modeling predicted that <sup>bull</sup>OH production occurs in a burst, regulated mainly by ammonium and ferric iron concentrations. We propose that the production of <sup>bull</sup>OH and extracellular proteolytic enzymes are regulated by similar nutritional signals. Oxidation works in concert with proteolysis, improving N liberation from proteins in SOM. Organic N mining by ectomycorrhizal fungi has, until now, only been attributed to proteolysis.</p>}},
  author       = {{Op De Beeck, Michiel and Troein, Carl and Peterson, Carsten and Persson, Per and Tunlid, Anders}},
  issn         = {{0028-646X}},
  keywords     = {{Fenton reaction; Nitrogen (N); Paxillus involutus; Proteolysis; Soil organic matter (SOM)}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{1}},
  pages        = {{335--343}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{New Phytologist}},
  title        = {{Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus}},
  url          = {{http://dx.doi.org/10.1111/nph.14971}},
  doi          = {{10.1111/nph.14971}},
  volume       = {{218}},
  year         = {{2018}},
}