Multi-omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring
2019
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 | Sichuan Academy of Agricultural Sciences | Ministry of Agriculture | Interactions Arbres-Microorganismes (IAM) ; Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL) | DOE Joint Genome Inst | University of California [Berkeley] (UC Berkeley) ; University of California (UC) | Architecture et fonction des macromolécules biologiques (AFMB) ; Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS) | Sichuan Science and Technology Program (Applied Fundamental Research Project) 2018JY0637 ; Special Fund for Agro-scientific Research in the Public Interest 201503137 ; Innovative Improvement Projects of Sichuan Province 2016ZYPZ-028 2019LWJJ-009 2016LWJJ-007 ; Key Breeding Project of Sichuan Province ; Laboratory of Excellence ARBRE, Region Lorraine, European Regional Development Fund ANR-11-LABX-0002-01 SAAS ; International Cooperation Fund 2015 ; United States Department of Energy (DOE) DE-AC02-05CH11231 | ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011)
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. Our findings contribute to an increasingly detailed portrait of molecular features triggering morel fruiting.
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