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Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow

BACKGROUND: The genus Streptococcus comprises pathogens that strongly influence the health of humans and animals. Genome sequencing of multiple Streptococcus strains demonstrated high variability in gene content and order even in closely related strains of the same species and created a newly emerge...

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Autores principales: Shelyakin, Pavel V., Bochkareva, Olga O., Karan, Anna A., Gelfand, Mikhail S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6437910/
https://www.ncbi.nlm.nih.gov/pubmed/30917781
http://dx.doi.org/10.1186/s12862-019-1403-6
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author Shelyakin, Pavel V.
Bochkareva, Olga O.
Karan, Anna A.
Gelfand, Mikhail S.
author_facet Shelyakin, Pavel V.
Bochkareva, Olga O.
Karan, Anna A.
Gelfand, Mikhail S.
author_sort Shelyakin, Pavel V.
collection PubMed
description BACKGROUND: The genus Streptococcus comprises pathogens that strongly influence the health of humans and animals. Genome sequencing of multiple Streptococcus strains demonstrated high variability in gene content and order even in closely related strains of the same species and created a newly emerged object for genomic analysis, the pan-genome. Here we analysed the genome evolution of 25 strains of Streptococcus suis, 50 strains of Streptococcus pyogenes and 28 strains of Streptococcus pneumoniae. RESULTS: Fractions of the pan-genome, unique, periphery, and universal genes differ in size, functional composition, the level of nucleotide substitutions, and predisposition to horizontal gene transfer and genomic rearrangements. The density of substitutions in intergenic regions appears to be correlated with selection acting on adjacent genes, implying that more conserved genes tend to have more conserved regulatory regions. The total pan-genome of the genus is open, but only due to strain-specific genes, whereas other pan-genome fractions reach saturation. We have identified the set of genes with phylogenies inconsistent with species and non-conserved location in the chromosome; these genes are rare in at least one species and have likely experienced recent horizontal transfer between species. The strain-specific fraction is enriched with mobile elements and hypothetical proteins, but also contains a number of candidate virulence-related genes, so it may have a strong impact on adaptability and pathogenicity. Mapping the rearrangements to the phylogenetic tree revealed large parallel inversions in all species. A parallel inversion of length 15 kB with breakpoints formed by genes encoding surface antigen proteins PhtD and PhtB in S. pneumoniae leads to replacement of gene fragments that likely indicates the action of an antigen variation mechanism. CONCLUSIONS: Members of genus Streptococcus have a highly dynamic, open pan-genome, that potentially confers them with the ability to adapt to changing environmental conditions, i.e. antibiotic resistance or transmission between different hosts. Hence, integrated analysis of all aspects of genome evolution is important for the identification of potential pathogens and design of drugs and vaccines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1403-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-64379102019-04-08 Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow Shelyakin, Pavel V. Bochkareva, Olga O. Karan, Anna A. Gelfand, Mikhail S. BMC Evol Biol Research Article BACKGROUND: The genus Streptococcus comprises pathogens that strongly influence the health of humans and animals. Genome sequencing of multiple Streptococcus strains demonstrated high variability in gene content and order even in closely related strains of the same species and created a newly emerged object for genomic analysis, the pan-genome. Here we analysed the genome evolution of 25 strains of Streptococcus suis, 50 strains of Streptococcus pyogenes and 28 strains of Streptococcus pneumoniae. RESULTS: Fractions of the pan-genome, unique, periphery, and universal genes differ in size, functional composition, the level of nucleotide substitutions, and predisposition to horizontal gene transfer and genomic rearrangements. The density of substitutions in intergenic regions appears to be correlated with selection acting on adjacent genes, implying that more conserved genes tend to have more conserved regulatory regions. The total pan-genome of the genus is open, but only due to strain-specific genes, whereas other pan-genome fractions reach saturation. We have identified the set of genes with phylogenies inconsistent with species and non-conserved location in the chromosome; these genes are rare in at least one species and have likely experienced recent horizontal transfer between species. The strain-specific fraction is enriched with mobile elements and hypothetical proteins, but also contains a number of candidate virulence-related genes, so it may have a strong impact on adaptability and pathogenicity. Mapping the rearrangements to the phylogenetic tree revealed large parallel inversions in all species. A parallel inversion of length 15 kB with breakpoints formed by genes encoding surface antigen proteins PhtD and PhtB in S. pneumoniae leads to replacement of gene fragments that likely indicates the action of an antigen variation mechanism. CONCLUSIONS: Members of genus Streptococcus have a highly dynamic, open pan-genome, that potentially confers them with the ability to adapt to changing environmental conditions, i.e. antibiotic resistance or transmission between different hosts. Hence, integrated analysis of all aspects of genome evolution is important for the identification of potential pathogens and design of drugs and vaccines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1403-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-27 /pmc/articles/PMC6437910/ /pubmed/30917781 http://dx.doi.org/10.1186/s12862-019-1403-6 Text en © The Author(s) 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Shelyakin, Pavel V.
Bochkareva, Olga O.
Karan, Anna A.
Gelfand, Mikhail S.
Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title_full Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title_fullStr Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title_full_unstemmed Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title_short Micro-evolution of three Streptococcus species: selection, antigenic variation, and horizontal gene inflow
title_sort micro-evolution of three streptococcus species: selection, antigenic variation, and horizontal gene inflow
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6437910/
https://www.ncbi.nlm.nih.gov/pubmed/30917781
http://dx.doi.org/10.1186/s12862-019-1403-6
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