Microbiome Community Structure and Functional Gene Partitioning in Different Micro-Niches Within a Sporocarp-Forming Fungus

Abstract

Thelephora ganbajun is a wild edible mushroom highly appreciated throughout China. The microbiomes of some fungal sporocarps have been studied, however, their potential functional roles currently remain uncharacterized. Here, functional gene microarrays (GeoChip 5.0) and amplicon sequencing were employed to define the taxonomic and functional attributes within three micro-niches of T. ganbajun. The diversity and composition of bacterial taxa and their functional genes differed significantly (p < 0.01) among the compartments. Among 31,117 functional genes detected, some were exclusively recorded in one sporocarp compartment: 1,334 genes involved in carbon (mdh) and nitrogen fixation (nifH) in the context; 524 genes influencing carbon (apu) and sulfite reduction (dsrB, dsra) in the hymenophore; and 255 genes involved in sulfur oxidation (soxB and soxC) and polyphosphate degradation (ppx) in the pileipellis. These results shed light on a previously unknown microbiome and functional gene partitioning in sporome compartments of Basidiomycota. This also has great implications for their potential ecological and biogeochemical functions, demonstrating a higher genomic complexity than previously thought.

Distinct Compartmentalization of Microbial Community and Potential Metabolic Function in the Fruiting Body of Tricholoma matsutake

“…Generally, more microbial species tended to inhabit the inner layer of T. matsutake as compared to the outer layer. This trend of higher microbial diversity at the inner layer was also found for another EMF, Thelephora ganbajun (also belonging to phylum Basidiomycota) [3].…”

“…Micro-niche partitioning disparity of the T. matsutake individual compartments (outer vs. inner layer), which assembles unique microbiomes, may explain this difference. Similar spatial niche-induced microbial recruitment and assembling trends were reported previously among fungus-associated components [39,40] and within fungus fruiting body parts [3,41]. Such strong and clear differences led us to explore the putative functions performed by the spatially distinct microbiomes in the EMF fungal fruiting body.…”

“…In a recent investigation by Liu et al (2021), while studying microbial functional gene compartmentalization in the EMF T. ganbajun, the thick interior context of the fungal fruiting body was found to have a greater abundance of C-and N-fixing genes, and sourcing energy and nutrition to the associated microbes [3]. Similarly, in the present study, the pileum context of T. matsutake may function as (i) an important reservoir of nutrients and (ii) a microbial hotspot niche as indicated by its highest microbial richness, in comparison to the other compartments of the fruiting body.…”

“…Nearly 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].…”

“…Unlike bacterial-fungal interactions, very little attention has been given to yeasts or filamentous fungi associated with basidiomata. To date, there is only one study related to the fungal microbiome distribution in the microniches of basidiomata-forming fungi [3]. Using functional gene analysis, Liu et al (2021) found that Monographella, Scytalidium, and Vanrija were correlated with functional gene structure in the context; Aspergillus and Lecanicillium were associated with the hymenophore; and Trichosporon were significantly (p < 0.01) associated with the pileipellis of Thelephora ganbajun (Thelephorales, Basidiomycota) [3].…”