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Decomposition of soil organic matter by ectomycorrhizal fungi : Mechanisms and consequences for organic nitrogen uptake and soil carbon stabilization

Tunlid, Anders LU ; Floudas, Dimitrios LU ; Op De Beeck, Michiel LU orcid ; Wang, Tao LU and Persson, Per LU (2022) In Frontiers in Forests and Global Change 5.
Abstract

A major fraction of nitrogen (N) in boreal forest soils is found in organic forms associated with soil organic matter (SOM) and mineral particles. The capacity of ectomycorrhizal (ECM) fungal symbionts to access this N is debated, considering that these fungi have lost many of the genes for decomposing organic matter that were present in their saprotrophic ancestors. To gain a molecular-level understanding of the N-mining processes in ECM fungi, we developed an experimental approach where the processes of decomposition were studied in parallel with the changes in the structure and properties of the organic matter. We showed that ECM fungi have significant capacities to assimilate organic N associated with SOM and mineral surfaces. The... (More)

A major fraction of nitrogen (N) in boreal forest soils is found in organic forms associated with soil organic matter (SOM) and mineral particles. The capacity of ectomycorrhizal (ECM) fungal symbionts to access this N is debated, considering that these fungi have lost many of the genes for decomposing organic matter that were present in their saprotrophic ancestors. To gain a molecular-level understanding of the N-mining processes in ECM fungi, we developed an experimental approach where the processes of decomposition were studied in parallel with the changes in the structure and properties of the organic matter. We showed that ECM fungi have significant capacities to assimilate organic N associated with SOM and mineral surfaces. The decomposition mechanisms differ between species, reflecting the lignocellulose decomposition mechanisms found in their saprotrophic ancestors. During N-mining, the ECM fungi processed the SOM to a material with increased adsorptive properties to iron oxide mineral particles. Two pathways contributed to these changes: Extracellular modifications of the SOM and secretion of mineral surface reactive metabolites. Some of these metabolites have iron(III)-reducing activities and can participate in extracellular Fenton reactions and redox reactions at iron oxide mineral surfaces. We conclude that the traditional framework for understanding organic N acquisition by ECM fungi from recalcitrant SOM must be extended to a framework that includes how those decomposition activities affect the stabilization and reactivity of mineral-associated SOM. The activity through these complex networks of reactions is decisive for the overall effect of ECM fungal decomposition on nutrients and C-cycling in forest ecosystems.

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; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
decomposition, ectomycorrhizal fungi, iron oxide minerals, metabolites, nitrogen acquisition, soil C stabilization
in
Frontiers in Forests and Global Change
volume
5
article number
934409
publisher
Frontiers Media S. A.
external identifiers
  • scopus:85135468918
ISSN
2624-893X
DOI
10.3389/ffgc.2022.934409
language
English
LU publication?
yes
id
9af2a97d-19ba-4214-9697-a6e59259f54c
date added to LUP
2022-09-20 14:40:13
date last changed
2024-05-16 19:26:38
@article{9af2a97d-19ba-4214-9697-a6e59259f54c,
  abstract     = {{<p>A major fraction of nitrogen (N) in boreal forest soils is found in organic forms associated with soil organic matter (SOM) and mineral particles. The capacity of ectomycorrhizal (ECM) fungal symbionts to access this N is debated, considering that these fungi have lost many of the genes for decomposing organic matter that were present in their saprotrophic ancestors. To gain a molecular-level understanding of the N-mining processes in ECM fungi, we developed an experimental approach where the processes of decomposition were studied in parallel with the changes in the structure and properties of the organic matter. We showed that ECM fungi have significant capacities to assimilate organic N associated with SOM and mineral surfaces. The decomposition mechanisms differ between species, reflecting the lignocellulose decomposition mechanisms found in their saprotrophic ancestors. During N-mining, the ECM fungi processed the SOM to a material with increased adsorptive properties to iron oxide mineral particles. Two pathways contributed to these changes: Extracellular modifications of the SOM and secretion of mineral surface reactive metabolites. Some of these metabolites have iron(III)-reducing activities and can participate in extracellular Fenton reactions and redox reactions at iron oxide mineral surfaces. We conclude that the traditional framework for understanding organic N acquisition by ECM fungi from recalcitrant SOM must be extended to a framework that includes how those decomposition activities affect the stabilization and reactivity of mineral-associated SOM. The activity through these complex networks of reactions is decisive for the overall effect of ECM fungal decomposition on nutrients and C-cycling in forest ecosystems.</p>}},
  author       = {{Tunlid, Anders and Floudas, Dimitrios and Op De Beeck, Michiel and Wang, Tao and Persson, Per}},
  issn         = {{2624-893X}},
  keywords     = {{decomposition; ectomycorrhizal fungi; iron oxide minerals; metabolites; nitrogen acquisition; soil C stabilization}},
  language     = {{eng}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Forests and Global Change}},
  title        = {{Decomposition of soil organic matter by ectomycorrhizal fungi : Mechanisms and consequences for organic nitrogen uptake and soil carbon stabilization}},
  url          = {{http://dx.doi.org/10.3389/ffgc.2022.934409}},
  doi          = {{10.3389/ffgc.2022.934409}},
  volume       = {{5}},
  year         = {{2022}},
}