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Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus.

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.

SUBMITTER: Op De Beeck M

PROVIDER: S-EPMC5873446 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus.

Op De Beeck Michiel M Troein Carl C Peterson Carsten C Persson Per P Tunlid Anders A

The New phytologist 20180103 1

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>˙</sup> OH), produced by the ectomycorrhizal fungus Paxillus involutus during growth ...[more]

PMID: 29297591

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Project description:The interactions between dissolved organic matter (DOM) and mineral particles are critical for the stabilization of soil organic matter (SOM) in terrestrial ecosystems. The processing of DOM by ectomycorrhizal fungi contributes to the formation of mineral-stabilized SOM by two contrasting pathways: the extracellular transformation of DOM (ex vivo pathway) and the secretion of mineral-surface-reactive metabolites (in vivo pathway). In this study, we examined how changes in nitrogen (N) availability affected the formation of mineral-associated carbon (C) from these two pathways. DOM was extracted from forest soils. The processing of this DOM by the ectomycorrhizal fungus Paxillus involutus was examined in laboratory-scale studies with different levels of ammonium. At low levels of ammonium (i.e., under N-limited conditions), the DOM components were slightly oxidized, and fungal C metabolites with iron-reducing activity were secreted. Ammonium amendments decreased the amount of C metabolites, and no additional oxidation of the organic matter was detected. In contrast, the hydrolytic activity and the secretion of N-containing compounds increased, particularly when high levels of ammonium were added. Under these conditions, C, but not N, limited fungal growth. Although the overall production of mineral-associated organic C was not affected by ammonium concentrations, the observed shifts in the activities of the ex vivo and in vivo pathways affected the composition of organic matter adsorbed onto the mineral particles. Such changes will affect the properties of organic matter-mineral associations and, thus, ultimately, the stabilization of SOM.IMPORTANCE Nitrogen (N) availability plays a critical role in the cycling and storage of soil organic matter (SOM). However, large uncertainties remain in predicting the net effect of N addition on soil organic carbon (C) storage due to the complex interactions between organic matter, microbial activity, and mineral particles that determine the formation of stable SOM. Here, we attempted to disentangle the effects of ammonium on these interactions in controlled microcosm experiments including the ectomycorrhizal fungus P. involutus and dissolved organic matter extracted from forest soils. Increased ammonium levels affected the fungal processing of the organic material as well as the secretion of extracellular metabolites. Although ammonium additions did not increase the net production of mineral-adsorbed C, changes in the decomposition and secretion pathways altered the composition of the adsorbed organic matter. These changes may influence the properties of the organic matter-mineral associations and, thus, the stabilization of SOM.

Dataset Information

Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus.

Publications

Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus.

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