Genomic insights into the evolution and adaptation of secondary metabolite gene clusters in fungicolous species Cladobotryum mycophilum ATHUM6906

Abstract

Mycophilic or fungicolous fungi can be found wherever fungi exist since they are able to colonize other fungi, which occupy a diverse range of habitats. Some fungicolous species cause important diseases on Basidiomycetes, and thus, they are the main reason for the destruction of mushroom cultivations. Nonetheless, despite their ecological significance, their genomic data remain limited. Cladobotryum mycophilum is one of the most aggressive species of the genus, destroying the economically important Agaricus bisporus cultivations. The 40.7 Mb whole genome of the Greek isolate ATHUM6906 is assembled in 16 fragments, including the mitochondrial genome and 2 small circular mitochondrial plasmids, in this study. This genome includes a comprehensive set of 12,282 protein coding, 56 rRNA, and 273 tRNA genes. Transposable elements, CAZymes, and pathogenicity related genes were also examined. The genome of C. mycophilum contained a diverse arsenal of genes involved in secondary metabolism, forming 106 biosynthetic gene clusters, which renders this genome as one of the most BGC abundant among fungicolous species. Comparative analyses were performed for genomes of species of the family Hypocreaceae. Some BGCs identified in C. mycophilum genome exhibited similarities to clusters found in the family Hypocreaceae, suggesting vertical heritage. In contrast, certain BGCs showed a scattered distribution among Hypocreaceae species or were solely found in Cladobotryum genomes. This work provides evidence of extensive BGC losses, horizontal gene transfer events, and formation of novel BGCs during evolution, potentially driven by neutral or even positive selection pressures. These events may increase Cladobotryum fitness under various environmental conditions and potentially during host-fungus interaction.

Keywords: Cladobotryum mycophilum; biosynthetic gene cluster (BGC); fungicolous fungi; genome; horizontal gene transfer (HGT); secondary metabolism.