The Architecture of Metabolism Maximizes Biosynthetic Diversity in the Largest Class of Fungi

Abstract

<jats:title>Abstract</jats:title> <jats:p>Ecological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or “specialized” metabolites (SMs) that mediate interactions with other organisms. Fungal SM pathways are frequently encoded in biosynthetic gene clusters (BGCs), which facilitate the identification and characterization of metabolic pathways. Variation in BGC composition reflects the diversity of their SM products. Recent studies have documented surprising diversity of BGC repertoires among isolates of the same fungal species, yet little is known about how this population-level variation is inherited across macroevolutionary timescales. Here, we applied a novel linkage-based algorithm to reveal previously unexplored dimensions of diversity in BGC composition, distribution, and repertoire across 101 species of Dothideomycetes, which are considered the most phylogenetically diverse class of fungi and known to produce many SMs. We predicted both complementary and overlapping sets of clustered genes compared with existing methods and identified novel gene pairs that associate with known secondary metabolite genes. We found that variation among sets of BGCs in individual genomes is due to nonoverlapping BGC combinations and that several BGCs have biased ecological distributions, consistent with niche-specific selection. We observed that total BGC diversity scales linearly with increasing repertoire size, suggesting that secondary metabolites have little structural redundancy in individual fungi. We project that there is substantial unsampled BGC diversity across specific families of Dothideomycetes, which will provide a roadmap for future sampling efforts. Our approach and findings lend new insight into how BGC diversity is generated and maintained across an entire fungal taxonomic class.</jats:p>

Depside and Depsidone Synthesis in Lichenized Fungi Comes into Focus through a Genome-Wide Comparison of the Olivetoric Acid and Physodic Acid Chemotypes of Pseudevernia furfuracea

“…We combine here our results with those of Watanabe and Townsend [75], Armaleo et al [10], Feng et al [12], Lünne et al [48], and Kealey et al [18], to provide an updated scheme of orcinol depside and depsidone synthesis, using as example the synthesis of olivetoric acid and physodic acid. We limit our description to orcinol lichen compounds as we do not yet know how many of the same rules apply to ß-orcinol depsides and depsidones.…”

Secondary metabolism drives ecological breadth in the Xylariaceae

“…Across 96 xylarialean genomes we predicted a total of 6,879 putative SMGCs (belonging to 3,313 cluster families) and 973 putative CGCs (belonging to 190 cluster families) (Supplementary Tables 3,4). In comparison, recent large-scale analyses predicted 3,399 SMGCs (in 719 cluster families) across 101 Dothideomycetes genomes 28 and 1,110 CGCs across 341 fungal genomes 29 . Only 25% of predicted SMGCs (n = 1,711, belonging to 816 cluster families) had BLAST hits to 168 unique MIBiG 30 accession numbers (Supplementary Table 3b).…”

Comparative Genomics and Transcriptomics Depict Marine Algicolous Arthrinium Species as Endosymbionts That Help Regulate Oxidative Stress in Brown Algae

“…are associated with virulence, except for pyranonigrin E, which is found only in A. phaeospermum. A previous study has suggested that alternapyrone and dimethylcoprogen play roles in plant pathogenesis (Gluck-Thaler et al, 2020). Dimethylcoprogen, a fungal extracellular siderophore, was reported to be responsible for the pathogenicity of Alternaria alternata to citrus (Chen L. H. et al, 2014).…”