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Functional genomics gives new insights into the ectomycorrhizal degradation of chitin

Maillard, François LU ; Kohler, Annegret ; Morin, Emmanuelle ; Hossann, Christian ; Miyauchi, Shingo ; Ziegler-Devin, Isabelle ; Gérant, Dominique ; Angeli, Nicolas ; Lipzen, Anna and Keymanesh, Keykhosrow , et al. (2023) In New Phytologist 238(2). p.845-858
Abstract

Ectomycorrhizal (EcM) fungi play a crucial role in the mineral nitrogen (N) nutrition of their host trees. While it has been proposed that several EcM species also mobilize organic N, studies reporting the EcM ability to degrade N-containing polymers, such as chitin, remain scarce. Here, we assessed the capacity of a representative collection of 16 EcM species to acquire 15N from 15N-chitin. In addition, we combined genomics and transcriptomics to identify pathways involved in exogenous chitin degradation between these fungal strains. Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum efficiently mobilized N from exogenous chitin. EcM genomes primarily contained genes encoding for the direct... (More)

Ectomycorrhizal (EcM) fungi play a crucial role in the mineral nitrogen (N) nutrition of their host trees. While it has been proposed that several EcM species also mobilize organic N, studies reporting the EcM ability to degrade N-containing polymers, such as chitin, remain scarce. Here, we assessed the capacity of a representative collection of 16 EcM species to acquire 15N from 15N-chitin. In addition, we combined genomics and transcriptomics to identify pathways involved in exogenous chitin degradation between these fungal strains. Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum efficiently mobilized N from exogenous chitin. EcM genomes primarily contained genes encoding for the direct hydrolysis of chitin. Further, we found a significant relationship between the capacity of EcM fungi to assimilate organic N from chitin and their genomic and transcriptomic potentials for chitin degradation. These findings demonstrate that certain EcM fungal species depolymerize chitin using hydrolytic mechanisms and that endochitinases, but not exochitinases, represent the enzymatic bottleneck of chitin degradation. Finally, this study shows that the degradation of exogenous chitin by EcM fungi might be a key functional trait of nutrient cycling in forests dominated by EcM fungi.

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publishing date
type
Contribution to journal
publication status
published
keywords
carbohydrate-active enzymes, endochitinase, exochitinase, GH18, GH20, organic nitrogen acquisition
in
New Phytologist
volume
238
issue
2
pages
14 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:85148515140
  • pmid:36702619
ISSN
0028-646X
DOI
10.1111/nph.18773
language
English
LU publication?
no
additional info
Publisher Copyright: © 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation Some of the authors are U.S. Government employees and their work is in the public domain in the USA.
id
4a7eb418-901f-4f1a-8cc1-7765bf9348b1
date added to LUP
2024-06-02 15:10:48
date last changed
2024-06-16 15:51:17
@article{4a7eb418-901f-4f1a-8cc1-7765bf9348b1,
  abstract     = {{<p>Ectomycorrhizal (EcM) fungi play a crucial role in the mineral nitrogen (N) nutrition of their host trees. While it has been proposed that several EcM species also mobilize organic N, studies reporting the EcM ability to degrade N-containing polymers, such as chitin, remain scarce. Here, we assessed the capacity of a representative collection of 16 EcM species to acquire <sup>15</sup>N from <sup>15</sup>N-chitin. In addition, we combined genomics and transcriptomics to identify pathways involved in exogenous chitin degradation between these fungal strains. Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum efficiently mobilized N from exogenous chitin. EcM genomes primarily contained genes encoding for the direct hydrolysis of chitin. Further, we found a significant relationship between the capacity of EcM fungi to assimilate organic N from chitin and their genomic and transcriptomic potentials for chitin degradation. These findings demonstrate that certain EcM fungal species depolymerize chitin using hydrolytic mechanisms and that endochitinases, but not exochitinases, represent the enzymatic bottleneck of chitin degradation. Finally, this study shows that the degradation of exogenous chitin by EcM fungi might be a key functional trait of nutrient cycling in forests dominated by EcM fungi.</p>}},
  author       = {{Maillard, François and Kohler, Annegret and Morin, Emmanuelle and Hossann, Christian and Miyauchi, Shingo and Ziegler-Devin, Isabelle and Gérant, Dominique and Angeli, Nicolas and Lipzen, Anna and Keymanesh, Keykhosrow and Johnson, Jenifer and Barry, Kerrie and Grigoriev, Igor V. and Martin, Francis M. and Buée, Marc}},
  issn         = {{0028-646X}},
  keywords     = {{carbohydrate-active enzymes; endochitinase; exochitinase; GH18; GH20; organic nitrogen acquisition}},
  language     = {{eng}},
  number       = {{2}},
  pages        = {{845--858}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{New Phytologist}},
  title        = {{Functional genomics gives new insights into the ectomycorrhizal degradation of chitin}},
  url          = {{http://dx.doi.org/10.1111/nph.18773}},
  doi          = {{10.1111/nph.18773}},
  volume       = {{238}},
  year         = {{2023}},
}