Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex

ABSTRACT Microbes produce a plethora of secondary (or specialized) metabolites that, although not essential for primary metabolism, benefit them to survive in the environment, communicate, and influence cell differentiation. Biosynthetic gene clusters (BGCs), responsible for the production of these...

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Autores principales:	Kat Steinke, Omkar S. Mohite, Tilmann Weber, Ákos T. Kovács
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Bacillus biosynthetic gene clusters fengycin iturin phylogeny plipastatin Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8836447b2a494c64bfe8f988cc150ef7
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spelling	oai:doaj.org-article:8836447b2a494c64bfe8f988cc150ef72021-12-02T17:07:47ZPhylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex10.1128/mSystems.00057-212379-5077https://doaj.org/article/8836447b2a494c64bfe8f988cc150ef72021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00057-21https://doaj.org/toc/2379-5077ABSTRACT Microbes produce a plethora of secondary (or specialized) metabolites that, although not essential for primary metabolism, benefit them to survive in the environment, communicate, and influence cell differentiation. Biosynthetic gene clusters (BGCs), responsible for the production of these secondary metabolites, are readily identifiable on bacterial genome sequences. Understanding the phylogeny and distribution of BGCs helps us to predict the natural product synthesis ability of new isolates. Here, we examined 310 genomes from the Bacillus subtilis group, determined the inter- and intraspecies patterns of absence/presence for all BGCs, and assigned them to defined gene cluster families (GCFs). This allowed us to establish patterns in the distribution of both known and unknown products. Further, we analyzed variations in the BGC structures of particular families encoding natural products, such as plipastatin, fengycin, iturin, mycosubtilin, and bacillomycin. Our detailed analysis revealed multiple GCFs that are species or clade specific and a few others that are scattered within or between species, which will guide exploration of the chemodiversity within the B. subtilis group. Surprisingly, we discovered that partial deletion of BGCs and frameshift mutations in selected biosynthetic genes are conserved within phylogenetically related isolates, although isolated from around the globe. Our results highlight the importance of detailed genomic analysis of BGCs and the remarkable phylogenetically conserved erosion of secondary metabolite biosynthetic potential in the B. subtilis group. IMPORTANCE Members of the B. subtilis species complex are commonly recognized producers of secondary metabolites, among those, the production of antifungals, which makes them promising biocontrol strains. While there are studies examining the distribution of well-known secondary metabolites in Bacilli, intraspecies clade-specific distribution has not been systematically reported for the B. subtilis group. Here, we report the complete biosynthetic potential within the B. subtilis group to explore the distribution of the biosynthetic gene clusters and to reveal an exhaustive phylogenetic conservation of secondary metabolite production within Bacillus that supports the chemodiversity within this species complex. We identify that certain gene clusters acquired deletions of genes and particular frameshift mutations, rendering them inactive for secondary metabolite biosynthesis, a conserved genetic trait within phylogenetically conserved clades of certain species. The overview guides the assignment of the secondary metabolite production potential of newly isolated Bacillus strains based on genome sequence and phylogenetic relatedness.Kat SteinkeOmkar S. MohiteTilmann WeberÁkos T. KovácsAmerican Society for MicrobiologyarticleBacillusbiosynthetic gene clustersfengyciniturinphylogenyplipastatinMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus biosynthetic gene clusters fengycin iturin phylogeny plipastatin Microbiology QR1-502
spellingShingle	Bacillus biosynthetic gene clusters fengycin iturin phylogeny plipastatin Microbiology QR1-502 Kat Steinke Omkar S. Mohite Tilmann Weber Ákos T. Kovács Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
description	ABSTRACT Microbes produce a plethora of secondary (or specialized) metabolites that, although not essential for primary metabolism, benefit them to survive in the environment, communicate, and influence cell differentiation. Biosynthetic gene clusters (BGCs), responsible for the production of these secondary metabolites, are readily identifiable on bacterial genome sequences. Understanding the phylogeny and distribution of BGCs helps us to predict the natural product synthesis ability of new isolates. Here, we examined 310 genomes from the Bacillus subtilis group, determined the inter- and intraspecies patterns of absence/presence for all BGCs, and assigned them to defined gene cluster families (GCFs). This allowed us to establish patterns in the distribution of both known and unknown products. Further, we analyzed variations in the BGC structures of particular families encoding natural products, such as plipastatin, fengycin, iturin, mycosubtilin, and bacillomycin. Our detailed analysis revealed multiple GCFs that are species or clade specific and a few others that are scattered within or between species, which will guide exploration of the chemodiversity within the B. subtilis group. Surprisingly, we discovered that partial deletion of BGCs and frameshift mutations in selected biosynthetic genes are conserved within phylogenetically related isolates, although isolated from around the globe. Our results highlight the importance of detailed genomic analysis of BGCs and the remarkable phylogenetically conserved erosion of secondary metabolite biosynthetic potential in the B. subtilis group. IMPORTANCE Members of the B. subtilis species complex are commonly recognized producers of secondary metabolites, among those, the production of antifungals, which makes them promising biocontrol strains. While there are studies examining the distribution of well-known secondary metabolites in Bacilli, intraspecies clade-specific distribution has not been systematically reported for the B. subtilis group. Here, we report the complete biosynthetic potential within the B. subtilis group to explore the distribution of the biosynthetic gene clusters and to reveal an exhaustive phylogenetic conservation of secondary metabolite production within Bacillus that supports the chemodiversity within this species complex. We identify that certain gene clusters acquired deletions of genes and particular frameshift mutations, rendering them inactive for secondary metabolite biosynthesis, a conserved genetic trait within phylogenetically conserved clades of certain species. The overview guides the assignment of the secondary metabolite production potential of newly isolated Bacillus strains based on genome sequence and phylogenetic relatedness.
format	article
author	Kat Steinke Omkar S. Mohite Tilmann Weber Ákos T. Kovács
author_facet	Kat Steinke Omkar S. Mohite Tilmann Weber Ákos T. Kovács
author_sort	Kat Steinke
title	Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
title_short	Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
title_full	Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
title_fullStr	Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
title_full_unstemmed	Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex
title_sort	phylogenetic distribution of secondary metabolites in the <named-content content-type="genus-species">bacillus subtilis</named-content> species complex
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/8836447b2a494c64bfe8f988cc150ef7
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Phylogenetic Distribution of Secondary Metabolites in the <named-content content-type="genus-species">Bacillus subtilis</named-content> Species Complex

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