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High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.

Shigella are pathogens originating within the Escherichia lineage but frequently classified as a separate genus. Shigella genomes contain numerous insertion sequences (ISs) that lead to pseudogenisation of affected genes and an increase of non-homologous recombination. Here, we study 414 genomes of...

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Autores principales: Seferbekova, Zaira, Zabelkin, Alexey, Yakovleva, Yulia, Afasizhev, Robert, Dranenko, Natalia O., Alexeev, Nikita, Gelfand, Mikhail S., Bochkareva, Olga O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8072062/
https://www.ncbi.nlm.nih.gov/pubmed/33912145
http://dx.doi.org/10.3389/fmicb.2021.628622
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author Seferbekova, Zaira
Zabelkin, Alexey
Yakovleva, Yulia
Afasizhev, Robert
Dranenko, Natalia O.
Alexeev, Nikita
Gelfand, Mikhail S.
Bochkareva, Olga O.
author_facet Seferbekova, Zaira
Zabelkin, Alexey
Yakovleva, Yulia
Afasizhev, Robert
Dranenko, Natalia O.
Alexeev, Nikita
Gelfand, Mikhail S.
Bochkareva, Olga O.
author_sort Seferbekova, Zaira
collection PubMed
description Shigella are pathogens originating within the Escherichia lineage but frequently classified as a separate genus. Shigella genomes contain numerous insertion sequences (ISs) that lead to pseudogenisation of affected genes and an increase of non-homologous recombination. Here, we study 414 genomes of E. coli and Shigella strains to assess the contribution of genomic rearrangements to Shigella evolution. We found that Shigella experienced exceptionally high rates of intragenomic rearrangements and had a decreased rate of homologous recombination compared to pathogenic and non-pathogenic E. coli. The high rearrangement rate resulted in independent disruption of syntenic regions and parallel rearrangements in different Shigella lineages. Specifically, we identified two types of chromosomally encoded E3 ubiquitin-protein ligases acquired independently by all Shigella strains that also showed a high level of sequence conservation in the promoter and further in the 5′-intergenic region. In the only available enteroinvasive E. coli (EIEC) strain, which is a pathogenic E. coli with a phenotype intermediate between Shigella and non-pathogenic E. coli, we found a rate of genome rearrangements comparable to those in other E. coli and no functional copies of the two Shigella-specific E3 ubiquitin ligases. These data indicate that the accumulation of ISs influenced many aspects of genome evolution and played an important role in the evolution of intracellular pathogens. Our research demonstrates the power of comparative genomics-based on synteny block composition and an important role of non-coding regions in the evolution of genomic islands.
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spelling pubmed-80720622021-04-27 High Rates of Genome Rearrangements and Pathogenicity of Shigella spp. Seferbekova, Zaira Zabelkin, Alexey Yakovleva, Yulia Afasizhev, Robert Dranenko, Natalia O. Alexeev, Nikita Gelfand, Mikhail S. Bochkareva, Olga O. Front Microbiol Microbiology Shigella are pathogens originating within the Escherichia lineage but frequently classified as a separate genus. Shigella genomes contain numerous insertion sequences (ISs) that lead to pseudogenisation of affected genes and an increase of non-homologous recombination. Here, we study 414 genomes of E. coli and Shigella strains to assess the contribution of genomic rearrangements to Shigella evolution. We found that Shigella experienced exceptionally high rates of intragenomic rearrangements and had a decreased rate of homologous recombination compared to pathogenic and non-pathogenic E. coli. The high rearrangement rate resulted in independent disruption of syntenic regions and parallel rearrangements in different Shigella lineages. Specifically, we identified two types of chromosomally encoded E3 ubiquitin-protein ligases acquired independently by all Shigella strains that also showed a high level of sequence conservation in the promoter and further in the 5′-intergenic region. In the only available enteroinvasive E. coli (EIEC) strain, which is a pathogenic E. coli with a phenotype intermediate between Shigella and non-pathogenic E. coli, we found a rate of genome rearrangements comparable to those in other E. coli and no functional copies of the two Shigella-specific E3 ubiquitin ligases. These data indicate that the accumulation of ISs influenced many aspects of genome evolution and played an important role in the evolution of intracellular pathogens. Our research demonstrates the power of comparative genomics-based on synteny block composition and an important role of non-coding regions in the evolution of genomic islands. Frontiers Media S.A. 2021-04-12 /pmc/articles/PMC8072062/ /pubmed/33912145 http://dx.doi.org/10.3389/fmicb.2021.628622 Text en Copyright © 2021 Seferbekova, Zabelkin, Yakovleva, Afasizhev, Dranenko, Alexeev, Gelfand and Bochkareva. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Seferbekova, Zaira
Zabelkin, Alexey
Yakovleva, Yulia
Afasizhev, Robert
Dranenko, Natalia O.
Alexeev, Nikita
Gelfand, Mikhail S.
Bochkareva, Olga O.
High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title_full High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title_fullStr High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title_full_unstemmed High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title_short High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.
title_sort high rates of genome rearrangements and pathogenicity of shigella spp.
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8072062/
https://www.ncbi.nlm.nih.gov/pubmed/33912145
http://dx.doi.org/10.3389/fmicb.2021.628622
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