The architecture of metabolism maximizes biosynthetic diversity in the largest class of Fungi

Emile Gluck-Thaler, Sajeet Haridas, Manfred Binder, Igor V. Grigoriev, Pedro W. Crous, Joseph W. Spatafora, Kathryn Bushley, Jason C. Slot

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Pages (from-to)2838-2856
Number of pages19
JournalMolecular biology and evolution
Volume37
Issue number10
DOIs
StatePublished - Oct 1 2020

Bibliographical note

Funding Information:
Computational work by E.G.-T. was conducted using the resources of the Ohio Supercomputer Center. This work was supported by the National Science Foundation (DEB-1638999 to J.C.S.), the Fonds de Recherche du Qu?bec-Nature et Technologies (to E.G.-T.), and the Ohio State University Graduate School (to E.G.-T.). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy (Contract No. DE-AC02-05CH11231).

Publisher Copyright:
© 2020 The Author(s).

Keywords

  • Chemical ecology
  • Fungi
  • Gene cluster
  • Metabolism

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