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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Vydáno v:Molecular biology and evolution Ročník 37; číslo 10; s. 2838 - 2856
Hlavní autoři: Gluck-Thaler, Emile, Haridas, Sajeet, Binder, Manfred, Grigoriev, Igor V, Crous, Pedro W, Spatafora, Joseph W, Bushley, Kathryn, Slot, Jason C
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Oxford University Press 01.10.2020
Témata:
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
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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.
AbstractList 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.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.
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.
Author Haridas, Sajeet
Binder, Manfred
Bushley, Kathryn
Spatafora, Joseph W
Crous, Pedro W
Gluck-Thaler, Emile
Slot, Jason C
Grigoriev, Igor V
AuthorAffiliation m6 Westerdijk Fungal Biodiversity Institute , Utrecht, The Netherlands
m8 Department of Plant and Microbial Biology, University of Minnesota , Minneapolis, MN
m4 TechBase, R-Tech GmbH , Regensburg, Germany
m5 Department of Plant and Microbial Biology, University of California , Berkeley, Berkeley, CA
m7 Department of Botany and Plant Pathology, Oregon State University , Corvallis, OR
m2 Department of Biological Sciences, University of Pittsburgh , Pittsburgh, PA
m1 Department of Plant Pathology, The Ohio State University , Columbus, OH
m3 US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory , Berkeley, CA
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– name: m5 Department of Plant and Microbial Biology, University of California , Berkeley, Berkeley, CA
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– name: m7 Department of Botany and Plant Pathology, Oregon State University , Corvallis, OR
– name: m4 TechBase, R-Tech GmbH , Regensburg, Germany
– name: m8 Department of Plant and Microbial Biology, University of Minnesota , Minneapolis, MN
– name: m3 US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory , Berkeley, CA
– name: m2 Department of Biological Sciences, University of Pittsburgh , Pittsburgh, PA
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  surname: Gluck-Thaler
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  organization: Department of Plant Pathology, The Ohio State University, Columbus, OH
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  organization: US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA
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  fullname: Crous, Pedro W
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  orcidid: 0000-0001-6731-3405
  surname: Slot
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  email: slot.1@osu.edu
  organization: Department of Plant Pathology, The Ohio State University, Columbus, OH
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32421770$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/1619160$$D View this record in Osti.gov
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ContentType Journal Article
Copyright The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2020
The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2020
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CorporateAuthor Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
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1537-1719
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IsDoiOpenAccess true
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Issue 10
Keywords chemical ecology
metabolism
gene cluster
fungi
Language English
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Snippet Ecological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or “specialized” metabolites (SMs) that...
Ecological diversity in fungi is largely defined by metabolic traits, including the ability to produce secondary or "specialized" metabolites (SMs) that...
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SubjectTerms 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
Title The Architecture of Metabolism Maximizes Biosynthetic Diversity in the Largest Class of Fungi
URI https://www.ncbi.nlm.nih.gov/pubmed/32421770
https://www.proquest.com/docview/3171297708
https://www.proquest.com/docview/2404639357
https://www.osti.gov/servlets/purl/1619160
https://pubmed.ncbi.nlm.nih.gov/PMC7530617
Volume 37
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