Abstract
The uniquely compartmentalized fruiting body structure of the ectomycorrhizal fungus (EMF) Tricholoma matsutake, 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 T. matsutake. 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, Caulobacter, and Sphingomonas were the primary significant bacterial taxa within the different compartments of the dissected T. matsutake fruiting body. Non-parametric multivariate analysis of variance showed significant compartmental differences for both the bacterial and the fungal community structure within the T. matsutake 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 T. matsutake.
Highlights
Bacterial diversity indices (Simpson and Shannon) exhibited no significant differences among T. matsutake compartments, but bacterial richness indices were significantly highest in the pileum context, which was in accordance with the highest number of unique bacterial operational taxonomic units (OTUs) found there (499; Figure 2A)
Among different T. matsutake tissues, the bacterial richness was higher in the inner layer than in the outer layer (Table 1)
Based on our study of a selected model ectomycorrhizal fungus (EMF), Tricholoma matsutake, we demonstrated that EMF do not merely function as fruiting bodies for spore dispersal, and localize different microbial communities within their structures to generate microbial hotspots of varying importance and complexity
Summary
The fungal phylum Basidiomycota is one of the most diverse fungal groups, with a presence over a wide environmental range [1]. 31,000 species across different genera belong to the phylum and account for more than a quarter of all known species of Eumycota [2]. Basidiomycota play a crucial role in terrestrial ecosystems, with members belonging to important trophic modes such as the saprotrophs, pathogens, or ectomycorrhizal fungi (EMF) [3,4]. Dominant in forest ecosystems, EMF regulate plant health, nutrient exchange, and forest sustainability [5,6]. Many studies in recent years have demonstrated
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