The genome and microbiome of a dikaryotic fungus (Inocybe terrigena, Inocybaceae) revealed by metagenomics

Abstract

Recent advances in molecular methods have increased our understanding of various fungal symbioses. However, little is known about genomic and microbiome features of most uncultured symbiotic fungal clades. Here, we analysed the genome and microbiome of Inocybaceae (Agaricales, Basidiomycota), a largely uncultured ectomycorrhizal clade known to form symbiotic associations with a wide variety of plant species. We used metagenomic sequencing and assembly of dikaryotic fruiting-body tissues from Inocybe terrigena (Fr.) Kuyper, to classify fungal and bacterial genomic sequences, and obtained a nearly complete fungal genome containing 93% of core eukaryotic genes. Comparative genomics reveals that I. terrigena is more similar to ectomycorrhizal and brown rot fungi than to white rot fungi. The reduction in lignin degradation capacity has been independent from and significantly faster than in closely related ectomycorrhizal clades supporting that ectomycorrhizal symbiosis evolved independently in Inocybe. The microbiome of I. terrigena fruiting-bodies includes bacteria with known symbiotic functions in other fungal and non-fungal host environments, suggesting potential symbiotic functions of these bacteria in fungal tissues regardless of habitat conditions. Our study demonstrates the usefulness of direct metagenomics analysis of fruiting-body tissues for characterizing fungal genomes and microbiome.

Growing edible mushrooms: a conversation between bacteria and fungi

“…The microbiome of Inocybe terrigena (scaly fibre head) fruiting‐bodies also includes bacteria showing symbiotic functions, regardless of habitat conditions (Bahram et al ., ). Among the symbiotic bacteria reported by the cited authors to inhabit the I. terrigena basidiomes: the genus Pseudomonas is, as already reported above, associated with mushroom fructification (Colauto et al ., ), Pedobacter species are noted for carrying a large number and variety of antimicrobial resistance genes (Viana et al .…”

Microbiota Associated with Different Developmental Stages of the Dry Rot Fungus Serpula lacrymans

“…Only little is known about the natural bacterial and fungal interaction partners of S. lacrymans , although there are numerous fungal microbiome studies available [ 32 , 33 , 34 , 35 , 36 ]. So far, the analysis of the airborne fungal spores in S. lacrymans -damaged homes revealed the co-occurrence of the ligninolytic Donkioporia expansa and the mycoparasite T. viride [ 14 ].…”

Host genetic variation strongly influences the microbiome structure and function in fungal fruiting‐bodies

“…Alphaproteobacteria was the most common class in all of those ascomycetes. Considering its low abundance in the microbiome of the M. oreades and in most of the previously studied basidiomycetes (Kumari et al ., ; Pent, et al ., ; Bahram, et al ., ), the dominance of Alphaproteobacteria may be characteristic of below‐ground and/or ascomycetous fruiting‐bodies, but not of basidiomycetes with above‐ground fruiting‐bodies. In contrast, the class Actinobacteria is common in saprotrophic basidiomycetes (Zagriadskaia et al ., ), including M. oreades as shown here.…”

“…In contrast, the class Actinobacteria is common in saprotrophic basidiomycetes (Zagriadskaia et al ., ), including M. oreades as shown here. Although Actinobacteria inhabit fruiting‐bodies of several ectomycorrhizal ascomycetes (Barbieri et al ., ; Quandt et al ., ; Benucci and Bonito, ), they have been rarely identified in ectomycorrhizal basidiomycetes (Dahm et al ., ; Pent et al ., ; Bahram et al ., ). These data suggest that not only the nutritional mode but also the phylogenetic origin of the host fungus and the position of fruiting‐bodies either below or above the ground may have a significant impact on their microbiomes.…”