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

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 ide...

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Bibliographic Details
Published in:Molecular biology and evolution Vol. 37; no. 10; pp. 2838 - 2856
Main Authors: Gluck-Thaler, Emile, Haridas, Sajeet, Binder, Manfred, Grigoriev, Igor V, Crous, Pedro W, Spatafora, Joseph W, Bushley, Kathryn, Slot, Jason C
Format: Journal Article
Language:English
Published: United States Oxford University Press 01.10.2020
Subjects:
Algorithms
Ascomycota - genetics
Ascomycota - metabolism
BASIC BIOLOGICAL SCIENCES
Biosynthetic Pathways - genetics
chemical ecology
Composition
Discoveries
Dothideomycetes
Fungi
gene cluster
Gene clusters
Gene Regulatory Networks
Genes
Geographical distribution
Melanins - metabolism
Metabolic pathways
Metabolism
Metabolites
Molecular Sequence Annotation
Multigene Family
Naphthols - metabolism
Redundancy
Secondary metabolites
Variation
chemical ecology
metabolism
gene cluster
fungi
ISSN:0737-4038, 1537-1719, 1537-1719
Online Access:Get full text
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Summary: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.
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AC02-05CH11231; DEB-1638999
USDOE Office of Science (SC)
National Science Foundation (NSF)
ISSN:0737-4038
1537-1719
1537-1719
DOI:10.1093/molbev/msaa122