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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Veröffentlicht in:	Molecular biology and evolution Jg. 37; H. 10; S. 2838 - 2856
Hauptverfasser:	Gluck-Thaler, Emile, Haridas, Sajeet, Binder, Manfred, Grigoriev, Igor V, Crous, Pedro W, Spatafora, Joseph W, Bushley, Kathryn, Slot, Jason C
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Oxford University Press 01.10.2020
Schlagworte:	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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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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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.
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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
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