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Title: Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring

Abstract

The black morel (Morchella importuna Kuo, O'Donnell and Volk) was once an uncultivable wild mushroom, until the development of exogenous nutrient bag (ENB), making its agricultural production quite feasible and stable. To date, how the nutritional acquisition of the morel mycelium is fulfilled to trigger its fruiting remains unknown. To investigate the mechanisms involved in ENB decomposition, the genome of a cultivable morel strain (M. importuna SCYDJ1-A1) was sequenced and the genes coding for the decay apparatus were identified. Expression of the encoded carbohydrate-active enzymes (CAZymes) was then analyzed by metatranscriptomics and metaproteomics in combination with biochemical assays. The results show that a diverse set of hydrolytic and redox CAZymes secreted by the morel mycelium is the main force driving the substrate decomposition. Plant polysaccharides such as starch and cellulose present in ENB substrate (wheat grains plus rice husks) were rapidly degraded, whereas triglycerides were accumulated initially and consumed later. ENB decomposition led to a rapid increase in the organic carbon content in the surface soil of the mushroom bed, which was thereafter consumed during morel fruiting. In contrast to the high carbon consumption, no significant acquisition of nitrogen was observed. Finally, our findings contribute to an increasingly detailed portraitmore » of molecular features triggering morel fruiting.« less

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [3];  [3];  [3];  [4];  [2];  [5];  [5] more »;  [1];  [1];  [1];  [1];  [2] « less
  1. Sichuan Academy of Agricultural Sciences, Chengdu (China); Ministry of Agriculture, Chengdu (China)
  2. Univ. de Lorraine, Champenoux (France)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  4. US Department of Energy Joint Genome Institute Walnut Creek CA USA; Department of Plant and Microbial BiologyUniversity of California Berkeley Berkeley CA USA
  5. Aix‐Marseille Univ. (France); Inst. National de la Recherche Agronomique, Marseille (France); King Abdulaziz Univ. Jeddah (Saudi Arabia)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1603530
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
[ Journal Volume: 21; Journal Issue: 10]; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Tan, Hao, Kohler, Annegret, Miao, Renyun, Liu, Tianhai, Zhang, Qiang, Zhang, Bo, Jiang, Lin, Wang, Yong, Xie, Liyuan, Tang, Jie, Li, Xiaolin, Liu, Lixu, Grigoriev, Igor V., Daum, Chris, LaButti, Kurt, Lipzen, Anna, Kuo, Alan, Morin, Emmanuelle, Drula, Elodie, Henrissat, Bernard, Wang, Bo, Huang, Zhongqian, Gan, Bingcheng, Peng, Weihong, and Martin, Francis M. Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring. United States: N. p., 2019. Web. doi:10.1111/1462-2920.14741.
Tan, Hao, Kohler, Annegret, Miao, Renyun, Liu, Tianhai, Zhang, Qiang, Zhang, Bo, Jiang, Lin, Wang, Yong, Xie, Liyuan, Tang, Jie, Li, Xiaolin, Liu, Lixu, Grigoriev, Igor V., Daum, Chris, LaButti, Kurt, Lipzen, Anna, Kuo, Alan, Morin, Emmanuelle, Drula, Elodie, Henrissat, Bernard, Wang, Bo, Huang, Zhongqian, Gan, Bingcheng, Peng, Weihong, & Martin, Francis M. Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring. United States. doi:10.1111/1462-2920.14741.
Tan, Hao, Kohler, Annegret, Miao, Renyun, Liu, Tianhai, Zhang, Qiang, Zhang, Bo, Jiang, Lin, Wang, Yong, Xie, Liyuan, Tang, Jie, Li, Xiaolin, Liu, Lixu, Grigoriev, Igor V., Daum, Chris, LaButti, Kurt, Lipzen, Anna, Kuo, Alan, Morin, Emmanuelle, Drula, Elodie, Henrissat, Bernard, Wang, Bo, Huang, Zhongqian, Gan, Bingcheng, Peng, Weihong, and Martin, Francis M. Thu . "Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring". United States. doi:10.1111/1462-2920.14741.
@article{osti_1603530,
title = {Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring},
author = {Tan, Hao and Kohler, Annegret and Miao, Renyun and Liu, Tianhai and Zhang, Qiang and Zhang, Bo and Jiang, Lin and Wang, Yong and Xie, Liyuan and Tang, Jie and Li, Xiaolin and Liu, Lixu and Grigoriev, Igor V. and Daum, Chris and LaButti, Kurt and Lipzen, Anna and Kuo, Alan and Morin, Emmanuelle and Drula, Elodie and Henrissat, Bernard and Wang, Bo and Huang, Zhongqian and Gan, Bingcheng and Peng, Weihong and Martin, Francis M.},
abstractNote = {The black morel (Morchella importuna Kuo, O'Donnell and Volk) was once an uncultivable wild mushroom, until the development of exogenous nutrient bag (ENB), making its agricultural production quite feasible and stable. To date, how the nutritional acquisition of the morel mycelium is fulfilled to trigger its fruiting remains unknown. To investigate the mechanisms involved in ENB decomposition, the genome of a cultivable morel strain (M. importuna SCYDJ1-A1) was sequenced and the genes coding for the decay apparatus were identified. Expression of the encoded carbohydrate-active enzymes (CAZymes) was then analyzed by metatranscriptomics and metaproteomics in combination with biochemical assays. The results show that a diverse set of hydrolytic and redox CAZymes secreted by the morel mycelium is the main force driving the substrate decomposition. Plant polysaccharides such as starch and cellulose present in ENB substrate (wheat grains plus rice husks) were rapidly degraded, whereas triglycerides were accumulated initially and consumed later. ENB decomposition led to a rapid increase in the organic carbon content in the surface soil of the mushroom bed, which was thereafter consumed during morel fruiting. In contrast to the high carbon consumption, no significant acquisition of nitrogen was observed. Finally, our findings contribute to an increasingly detailed portrait of molecular features triggering morel fruiting.},
doi = {10.1111/1462-2920.14741},
journal = {Environmental Microbiology},
number = [10],
volume = [21],
place = {United States},
year = {2019},
month = {7}
}

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