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


Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
01 10 2020
Historique:
pubmed: 19 5 2020
medline: 16 4 2021
entrez: 19 5 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 32421770
pii: 5839751
doi: 10.1093/molbev/msaa122
pmc: PMC7530617
doi:

Substances chimiques

1,8-dihydroxynaphthalene melanin 0
Melanins 0
Naphthols 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

2838-2856

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Auteurs

Emile Gluck-Thaler (E)

Department of Plant Pathology, The Ohio State University, Columbus, OH.
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA.

Sajeet Haridas (S)

US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA.

Manfred Binder (M)

TechBase, R-Tech GmbH, Regensburg, Germany.

Igor V Grigoriev (IV)

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.

Pedro W Crous (PW)

Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.

Joseph W Spatafora (JW)

Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR.

Kathryn Bushley (K)

Department of Plant and Microbial Biology, University of Minnesota, Minneapolis, MN.

Jason C Slot (JC)

Department of Plant Pathology, The Ohio State University, Columbus, OH.

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