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Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin

BACKGROUND: Streptomyces are widespread bacteria that contribute to the terrestrial carbon cycle and produce the majority of clinically useful antibiotics. While interspecific genomic diversity has been investigated among Streptomyces, information is lacking on intraspecific genomic diversity. Strep...

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Autores principales: Doroghazi, James R, Buckley, Daniel H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4239341/
https://www.ncbi.nlm.nih.gov/pubmed/25399205
http://dx.doi.org/10.1186/1471-2164-15-970
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author Doroghazi, James R
Buckley, Daniel H
author_facet Doroghazi, James R
Buckley, Daniel H
author_sort Doroghazi, James R
collection PubMed
description BACKGROUND: Streptomyces are widespread bacteria that contribute to the terrestrial carbon cycle and produce the majority of clinically useful antibiotics. While interspecific genomic diversity has been investigated among Streptomyces, information is lacking on intraspecific genomic diversity. Streptomyces pratensis has high rates of homologous recombination but the impact of such gene exchange on genome evolution and the evolution of natural product gene clusters remains uncharacterized. RESULTS: We report draft genome sequences of four S. pratensis strains and compare to the complete genome of Streptomyces flavogriseus IAF-45-CD (=ATCC 33331), a strain recently reclassified to S. pratensis. Despite disparate geographic origins, the genomes are highly similar with 85.9% of genes present in the core genome and conservation of all natural product gene clusters. Natural products include a novel combination of carbapenem and beta-lactamase inhibitor gene clusters. While high intraspecies recombination rates abolish the phylogenetic signal across the genome, intraspecies recombination is suppressed in two genomic regions. The first region is centered on an insertion/deletion polymorphism and the second on a hybrid NRPS-PKS gene. Finally, two gene families accounted for over 25% of the divergent genes in the core genome. The first includes homologs of bldB (required for spore development and antibiotic production) while the second includes homologs of an uncharacterized protein with a helix-turn-helix motif (hpb). Genes from these families co-occur with fifteen pairs spread across the genome. These genes have evidence for co-evolution of co-localized pairs, supporting previous assertions that these genes may function akin to a toxin-antitoxin system. CONCLUSIONS: S. pratensis genomes are highly similar with exceptional levels of recombination which erase phylogenetic signal among strains of the species. This species has a large core genome and variable terminal regions that are smaller than those found in interspecies comparisons. There is no geographic differentiation between these strains, but there is evidence for local linkage disequilibrium affecting two genomic regions. We have also shown further observational evidence that the DUF397-HTH (bldB and hpb) are a novel toxin-antitoxin pair.
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spelling pubmed-42393412014-11-21 Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin Doroghazi, James R Buckley, Daniel H BMC Genomics Research Article BACKGROUND: Streptomyces are widespread bacteria that contribute to the terrestrial carbon cycle and produce the majority of clinically useful antibiotics. While interspecific genomic diversity has been investigated among Streptomyces, information is lacking on intraspecific genomic diversity. Streptomyces pratensis has high rates of homologous recombination but the impact of such gene exchange on genome evolution and the evolution of natural product gene clusters remains uncharacterized. RESULTS: We report draft genome sequences of four S. pratensis strains and compare to the complete genome of Streptomyces flavogriseus IAF-45-CD (=ATCC 33331), a strain recently reclassified to S. pratensis. Despite disparate geographic origins, the genomes are highly similar with 85.9% of genes present in the core genome and conservation of all natural product gene clusters. Natural products include a novel combination of carbapenem and beta-lactamase inhibitor gene clusters. While high intraspecies recombination rates abolish the phylogenetic signal across the genome, intraspecies recombination is suppressed in two genomic regions. The first region is centered on an insertion/deletion polymorphism and the second on a hybrid NRPS-PKS gene. Finally, two gene families accounted for over 25% of the divergent genes in the core genome. The first includes homologs of bldB (required for spore development and antibiotic production) while the second includes homologs of an uncharacterized protein with a helix-turn-helix motif (hpb). Genes from these families co-occur with fifteen pairs spread across the genome. These genes have evidence for co-evolution of co-localized pairs, supporting previous assertions that these genes may function akin to a toxin-antitoxin system. CONCLUSIONS: S. pratensis genomes are highly similar with exceptional levels of recombination which erase phylogenetic signal among strains of the species. This species has a large core genome and variable terminal regions that are smaller than those found in interspecies comparisons. There is no geographic differentiation between these strains, but there is evidence for local linkage disequilibrium affecting two genomic regions. We have also shown further observational evidence that the DUF397-HTH (bldB and hpb) are a novel toxin-antitoxin pair. BioMed Central 2014-11-15 /pmc/articles/PMC4239341/ /pubmed/25399205 http://dx.doi.org/10.1186/1471-2164-15-970 Text en © Doroghazi and Buckley; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Doroghazi, James R
Buckley, Daniel H
Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title_full Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title_fullStr Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title_full_unstemmed Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title_short Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
title_sort intraspecies comparison of streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4239341/
https://www.ncbi.nlm.nih.gov/pubmed/25399205
http://dx.doi.org/10.1186/1471-2164-15-970
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