Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus

New Phytol. 2018 Apr;218(1):335-343. doi: 10.1111/nph.14971. Epub 2018 Jan 3.

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 (˙ 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. ˙ OH production, ammonium assimilation, and proteolytic activity were measured daily. ˙ 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 ˙ OH production occurs in a burst, regulated mainly by ammonium and ferric iron concentrations. We propose that the production of ˙ 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.

Keywords: Paxillus involutus; Fenton reaction; nitrogen (N); proteolysis; soil organic matter (SOM).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agaricales / metabolism*
  • Aspartic Acid / metabolism
  • Fungal Proteins / metabolism
  • Hydrogen Peroxide / metabolism*
  • Hydroxyl Radical / metabolism
  • Iron / metabolism*
  • Models, Biological
  • Mycorrhizae / metabolism*
  • Nitrogen / metabolism*
  • Organic Chemicals / metabolism*
  • Oxidation-Reduction
  • Proteolysis

Substances

  • Fenton's reagent
  • Fungal Proteins
  • Organic Chemicals
  • Aspartic Acid
  • Hydroxyl Radical
  • Hydrogen Peroxide
  • Iron
  • Nitrogen