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Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus

A variety of secondary metabolites contributing to plant growth are synthesized by bacterial nonribosomal peptide synthases (NRPSs). Among them, the NRPS biosynthesis of surfactin is regulated by the SrfA operon. To explore the molecular mechanism for the diversity of surfactins produced by bacteria...

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Autores principales: Xu, Ying, Wu, Jia-Yi, Liu, Qing-Jie, Xue, Jia-Yu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9956979/
https://www.ncbi.nlm.nih.gov/pubmed/36833349
http://dx.doi.org/10.3390/genes14020422
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author Xu, Ying
Wu, Jia-Yi
Liu, Qing-Jie
Xue, Jia-Yu
author_facet Xu, Ying
Wu, Jia-Yi
Liu, Qing-Jie
Xue, Jia-Yu
author_sort Xu, Ying
collection PubMed
description A variety of secondary metabolites contributing to plant growth are synthesized by bacterial nonribosomal peptide synthases (NRPSs). Among them, the NRPS biosynthesis of surfactin is regulated by the SrfA operon. To explore the molecular mechanism for the diversity of surfactins produced by bacteria within the genus Bacillus, we performed a genome-wide identification study focused on three critical genes of the SrfA operon—SrfAA, SrfAB and SrfAC—from 999 Bacillus genomes (belonging to 47 species). Gene family clustering indicated the three genes can be divided into 66 orthologous groups (gene families), of which a majority comprised members of multiple genes (e.g., OG0000009 had members of all three SrfAA, SrfAB and SrfAC genes), indicating high sequence similarity among the three genes. Phylogenetic analyses also found that none of the three genes formed monophyletic groups, but were usually arranged in a mixed manner, suggesting the close evolutionary relationship among the three genes. Considering the module structure of the three genes, we propose that self-duplication, especially tandem duplications, might have contributed to the initial establishment of the entire SrfA operon, and further gene fusion and recombination as well as accumulated mutations might have continuously shaped the different functional roles of SrfAA, SrfAB and SrfAC. Overall, this study provides novel insight into metabolic gene clusters and operon evolution in bacteria.
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spelling pubmed-99569792023-02-25 Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus Xu, Ying Wu, Jia-Yi Liu, Qing-Jie Xue, Jia-Yu Genes (Basel) Communication A variety of secondary metabolites contributing to plant growth are synthesized by bacterial nonribosomal peptide synthases (NRPSs). Among them, the NRPS biosynthesis of surfactin is regulated by the SrfA operon. To explore the molecular mechanism for the diversity of surfactins produced by bacteria within the genus Bacillus, we performed a genome-wide identification study focused on three critical genes of the SrfA operon—SrfAA, SrfAB and SrfAC—from 999 Bacillus genomes (belonging to 47 species). Gene family clustering indicated the three genes can be divided into 66 orthologous groups (gene families), of which a majority comprised members of multiple genes (e.g., OG0000009 had members of all three SrfAA, SrfAB and SrfAC genes), indicating high sequence similarity among the three genes. Phylogenetic analyses also found that none of the three genes formed monophyletic groups, but were usually arranged in a mixed manner, suggesting the close evolutionary relationship among the three genes. Considering the module structure of the three genes, we propose that self-duplication, especially tandem duplications, might have contributed to the initial establishment of the entire SrfA operon, and further gene fusion and recombination as well as accumulated mutations might have continuously shaped the different functional roles of SrfAA, SrfAB and SrfAC. Overall, this study provides novel insight into metabolic gene clusters and operon evolution in bacteria. MDPI 2023-02-07 /pmc/articles/PMC9956979/ /pubmed/36833349 http://dx.doi.org/10.3390/genes14020422 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Communication
Xu, Ying
Wu, Jia-Yi
Liu, Qing-Jie
Xue, Jia-Yu
Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title_full Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title_fullStr Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title_full_unstemmed Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title_short Genome-Wide Identification and Evolutionary Analyses of SrfA Operon Genes in Bacillus
title_sort genome-wide identification and evolutionary analyses of srfa operon genes in bacillus
topic Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9956979/
https://www.ncbi.nlm.nih.gov/pubmed/36833349
http://dx.doi.org/10.3390/genes14020422
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