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Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates

Morels (Morchella sp.) are economically important edible macro-fungi, which can grow on various synthetic or semi-synthetic media. However, the complex nutritional metabolism and requirements of these fungi remain ill-defined. This study, based on the plant biomass commonly used in the artificial cu...

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Autores principales: Cai, YingLi, Ma, XiaoLong, Zhang, QianQian, Yu, FuQiang, Zhao, Qi, Huang, Wei, Song, JiaXin, Liu, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8185036/
https://www.ncbi.nlm.nih.gov/pubmed/34113321
http://dx.doi.org/10.3389/fmicb.2021.636344
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author Cai, YingLi
Ma, XiaoLong
Zhang, QianQian
Yu, FuQiang
Zhao, Qi
Huang, Wei
Song, JiaXin
Liu, Wei
author_facet Cai, YingLi
Ma, XiaoLong
Zhang, QianQian
Yu, FuQiang
Zhao, Qi
Huang, Wei
Song, JiaXin
Liu, Wei
author_sort Cai, YingLi
collection PubMed
description Morels (Morchella sp.) are economically important edible macro-fungi, which can grow on various synthetic or semi-synthetic media. However, the complex nutritional metabolism and requirements of these fungi remain ill-defined. This study, based on the plant biomass commonly used in the artificial cultivation of morels, assessed and compared the growth characteristics and extracellular enzymes of Morchella importuna cultivated on glucose, rice straw, sawdust, wheat grain, and a mixture of equal proportions of the three latter plant substrates (MIX). M. importuna could grow on all five tested media but displayed significant variations in mycelial growth rate, biomass, and sclerotium yield on the different media. The most suitable medium for M. importuna was wheat and wheat-containing medium, followed by glucose, while rice straw and sawdust were the least suitable. A total of 268 secretory proteins were identified by liquid chromatography coupled with tandem mass spectrometry detection. Functional classification and label-free comparative analysis of these proteins revealed that carbohydrate-active enzyme (CAZYme) proteins were the predominant component of the secretome of M. importuna, followed by protease, peptidase, and other proteins. The abundances of CAZYme proteins differed among the tested media, ranging from 64% on glucose to 88% on rice straw. The CAZYme classes of glycoside hydrolases and carbohydrate-binding module were enriched in the five secretomes. Furthermore, the enzyme activities of CMCase, lignase, amylase, xylase, pNPCase, and pNPGase were detected during the continuous culture of M. importuna in MIX medium, and the relative expression of the corresponding genes were detected by quantitative real-time PCR. The combined data of growth potential, secretome, extracellular enzyme activity, and gene expression on different substrates inferred that M. importuna was weak in lignocellulose degradation but a good starch decomposer. Specifically, in terms of the degradation of cellulose, the ability to degrade cellulose into oligosaccharides was weaker compared with further degradation into monosaccharides, and this might be the speed-limiting step of cellulose utilization in M. importuna. In addition, M. importuna had a strong ability to decompose various hemicellulose glycosidic bonds, especially α- and β-galactosidase. Only a very few lignin-degradation-related proteins were detected, and these were in low abundance, consistent with the presence of weak lignin degradation ability. Furthermore, the presence of lipase and chitinase implied that M. importuna was capable of decomposition of its own mycelia in vitro. The study provides key data that facilitates a further understanding of the complex nutritional metabolism of M. importuna.
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spelling pubmed-81850362021-06-09 Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates Cai, YingLi Ma, XiaoLong Zhang, QianQian Yu, FuQiang Zhao, Qi Huang, Wei Song, JiaXin Liu, Wei Front Microbiol Microbiology Morels (Morchella sp.) are economically important edible macro-fungi, which can grow on various synthetic or semi-synthetic media. However, the complex nutritional metabolism and requirements of these fungi remain ill-defined. This study, based on the plant biomass commonly used in the artificial cultivation of morels, assessed and compared the growth characteristics and extracellular enzymes of Morchella importuna cultivated on glucose, rice straw, sawdust, wheat grain, and a mixture of equal proportions of the three latter plant substrates (MIX). M. importuna could grow on all five tested media but displayed significant variations in mycelial growth rate, biomass, and sclerotium yield on the different media. The most suitable medium for M. importuna was wheat and wheat-containing medium, followed by glucose, while rice straw and sawdust were the least suitable. A total of 268 secretory proteins were identified by liquid chromatography coupled with tandem mass spectrometry detection. Functional classification and label-free comparative analysis of these proteins revealed that carbohydrate-active enzyme (CAZYme) proteins were the predominant component of the secretome of M. importuna, followed by protease, peptidase, and other proteins. The abundances of CAZYme proteins differed among the tested media, ranging from 64% on glucose to 88% on rice straw. The CAZYme classes of glycoside hydrolases and carbohydrate-binding module were enriched in the five secretomes. Furthermore, the enzyme activities of CMCase, lignase, amylase, xylase, pNPCase, and pNPGase were detected during the continuous culture of M. importuna in MIX medium, and the relative expression of the corresponding genes were detected by quantitative real-time PCR. The combined data of growth potential, secretome, extracellular enzyme activity, and gene expression on different substrates inferred that M. importuna was weak in lignocellulose degradation but a good starch decomposer. Specifically, in terms of the degradation of cellulose, the ability to degrade cellulose into oligosaccharides was weaker compared with further degradation into monosaccharides, and this might be the speed-limiting step of cellulose utilization in M. importuna. In addition, M. importuna had a strong ability to decompose various hemicellulose glycosidic bonds, especially α- and β-galactosidase. Only a very few lignin-degradation-related proteins were detected, and these were in low abundance, consistent with the presence of weak lignin degradation ability. Furthermore, the presence of lipase and chitinase implied that M. importuna was capable of decomposition of its own mycelia in vitro. The study provides key data that facilitates a further understanding of the complex nutritional metabolism of M. importuna. Frontiers Media S.A. 2021-05-25 /pmc/articles/PMC8185036/ /pubmed/34113321 http://dx.doi.org/10.3389/fmicb.2021.636344 Text en Copyright © 2021 Cai, Ma, Zhang, Yu, Zhao, Huang, Song and Liu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Cai, YingLi
Ma, XiaoLong
Zhang, QianQian
Yu, FuQiang
Zhao, Qi
Huang, Wei
Song, JiaXin
Liu, Wei
Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title_full Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title_fullStr Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title_full_unstemmed Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title_short Physiological Characteristics and Comparative Secretome Analysis of Morchella importuna Grown on Glucose, Rice Straw, Sawdust, Wheat Grain, and MIX Substrates
title_sort physiological characteristics and comparative secretome analysis of morchella importuna grown on glucose, rice straw, sawdust, wheat grain, and mix substrates
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8185036/
https://www.ncbi.nlm.nih.gov/pubmed/34113321
http://dx.doi.org/10.3389/fmicb.2021.636344
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