Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>

The uniquely compartmentalized fruiting body structure of the ectomycorrhizal fungus (EMF) <i>Tricholoma matsutake</i>, is a hotspot of microbial habitation and interaction. However, microbial diversity within this microniche structure of the EMF is rarely investigated. Furthermore, ther...

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Main Authors: Dong Liu, Jesús Perez-Moreno, Peng Zhang, Ran Wang, Caspar C. C. Chater, Fuqiang Yu
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/7/8/586
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author Dong Liu
Jesús Perez-Moreno
Peng Zhang
Ran Wang
Caspar C. C. Chater
Fuqiang Yu
author_facet Dong Liu
Jesús Perez-Moreno
Peng Zhang
Ran Wang
Caspar C. C. Chater
Fuqiang Yu
author_sort Dong Liu
collection DOAJ
description The uniquely compartmentalized fruiting body structure of the ectomycorrhizal fungus (EMF) <i>Tricholoma matsutake</i>, is a hotspot of microbial habitation and interaction. However, microbial diversity within this microniche structure of the EMF is rarely investigated. Furthermore, there is limited information concerning microbiomes associated with sporomes belonging to the ubiquitous fungal phylum Basidiomycota, particularly with respect to fungus-EMF interactions. In this study, we conducted high throughput sequencing, using ITS (fungal) and 16S rRNA (bacterial) marker genes to characterize and compare fruiting body microbiomes in the outer (pileipellis and stipitipellis) and inner layers (pileum context, stipe context, and lamellae) of the fruiting body of <i>T. matsutake</i>. Our results show the number of unique bacterial operational taxonomic units (OTUs) among the different compartments ranged from 410 to 499 and was more than double that of the shared/common OTUs (235). Micrococcales, Bacillales, <i>Caulobacter</i>, and <i>Sphingomonas</i> were the primary significant bacterial taxa within the different compartments of the dissected <i>T. matsutake</i> fruiting body. Non-parametric multivariate analysis of variance showed significant compartmental differences for both the bacterial and the fungal community structure within the <i>T. matsutake</i> fruiting body. The metabolic profiling revealed putative metabolisms (of amino acids, carbohydrates, and nucleotides) and the biosynthesis of secondary metabolites to be highly enriched in outer layers; in the inner parts, the metabolisms of energy, cofactors, vitamins, and lipids were significantly higher. This study demonstrates for the first time the distinct compartmentalization of microbial communities and potential metabolic function profiles in the fruiting body of an economically important EMF <i>T. matsutake</i>.
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spelling doaj.art-90d2dde4fec34668b0b5c86fa31f47812023-11-22T08:16:21ZengMDPI AGJournal of Fungi2309-608X2021-07-017858610.3390/jof7080586Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>Dong Liu0Jesús Perez-Moreno1Peng Zhang2Ran Wang3Caspar C. C. Chater4Fuqiang Yu5The Germplasm Bank of Wild Species, Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaColegio de Postgraduados, Campus Montecillo, Microbiología, Edafología, Texcoco 56230, MexicoThe Germplasm Bank of Wild Species, Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaThe Germplasm Bank of Wild Species, Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaDepartment of Natural Capital and Plant Health, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, UKThe Germplasm Bank of Wild Species, Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, ChinaThe uniquely compartmentalized fruiting body structure of the ectomycorrhizal fungus (EMF) <i>Tricholoma matsutake</i>, is a hotspot of microbial habitation and interaction. However, microbial diversity within this microniche structure of the EMF is rarely investigated. Furthermore, there is limited information concerning microbiomes associated with sporomes belonging to the ubiquitous fungal phylum Basidiomycota, particularly with respect to fungus-EMF interactions. In this study, we conducted high throughput sequencing, using ITS (fungal) and 16S rRNA (bacterial) marker genes to characterize and compare fruiting body microbiomes in the outer (pileipellis and stipitipellis) and inner layers (pileum context, stipe context, and lamellae) of the fruiting body of <i>T. matsutake</i>. Our results show the number of unique bacterial operational taxonomic units (OTUs) among the different compartments ranged from 410 to 499 and was more than double that of the shared/common OTUs (235). Micrococcales, Bacillales, <i>Caulobacter</i>, and <i>Sphingomonas</i> were the primary significant bacterial taxa within the different compartments of the dissected <i>T. matsutake</i> fruiting body. Non-parametric multivariate analysis of variance showed significant compartmental differences for both the bacterial and the fungal community structure within the <i>T. matsutake</i> fruiting body. The metabolic profiling revealed putative metabolisms (of amino acids, carbohydrates, and nucleotides) and the biosynthesis of secondary metabolites to be highly enriched in outer layers; in the inner parts, the metabolisms of energy, cofactors, vitamins, and lipids were significantly higher. This study demonstrates for the first time the distinct compartmentalization of microbial communities and potential metabolic function profiles in the fruiting body of an economically important EMF <i>T. matsutake</i>.https://www.mdpi.com/2309-608X/7/8/586<i>Tricholoma matsutake</i>ectomycorrhizal fungimicrobial partitioningmetabolic profilingBasidiomycotafruiting body
spellingShingle Dong Liu
Jesús Perez-Moreno
Peng Zhang
Ran Wang
Caspar C. C. Chater
Fuqiang Yu
Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
Journal of Fungi
<i>Tricholoma matsutake</i>
ectomycorrhizal fungi
microbial partitioning
metabolic profiling
Basidiomycota
fruiting body
title Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
title_full Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
title_fullStr Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
title_full_unstemmed Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
title_short Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of <i>Tricholoma matsutake</i>
title_sort distinct compartmentalization of microbial community and potential metabolic function in the fruiting body of i tricholoma matsutake i
topic <i>Tricholoma matsutake</i>
ectomycorrhizal fungi
microbial partitioning
metabolic profiling
Basidiomycota
fruiting body
url https://www.mdpi.com/2309-608X/7/8/586
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