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

Journal Article · Mon May 18 00:00:00 UTC 2020 · Molecular Biology and Evolution

DOI: https://doi.org/10.1093/molbev/msaa122 · OSTI ID:1703186

Gluck-Thaler, Emile ^[1]; Haridas, Sajeet ^[2]; Binder, Manfred ^[3]; Grigoriev, Igor V. ^[4]; Crous, Pedro W. ^[5]; Spatafora, Joseph W. ^[6]; Bushley, Kathryn ^[7]; Slot, Jason C.  ^[8]; Townsend, ed., Jeffrey

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1. Department of Plant Pathology, The Ohio State University, Columbus, OH, Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA
2. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA
3. TechBase, R-Tech GmbH, Regensburg, Germany
4. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA
5. Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands
6. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR
7. Department of Plant and Microbial Biology, University of Minnesota, Minneapolis, MN
8. Department of Plant Pathology, The Ohio State University, Columbus, OH

Abstract 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.

• Research Organization: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
• Sponsoring Organization: National Science Foundation (NSF); USDOE; USDOE Office of Science (SC)
• Grant/Contract Number: AC02-05CH11231
• OSTI ID: 1703186
• Journal Information: Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 10 Vol. 37; ISSN 0737-4038
• Publisher: Oxford University PressCopyright Statement
• Country of Publication: United States
• Language: English