TY - JOUR

T1 - High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.

AU - Сефербекова, Заира

AU - Забелкин, Алексей

AU - Яковлева, Юлия Александровна

AU - Афасижев, Роберт

AU - Драненко, Наталия

AU - Алексеев, Никита

AU - Гельфанд, Михаил

AU - Бочкарева, Ольга

N1 - Publisher Copyright: © Copyright © 2021 Seferbekova, Zabelkin, Yakovleva, Afasizhev, Dranenko, Alexeev, Gelfand and Bochkareva.

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

KW - E3 ubiquitin-ligases

KW - Escherichia coli

KW - IS

KW - Shigella

KW - pathogens

KW - rearrangements

KW - recombination

KW - SEQUENCES

KW - ESCHERICHIA-COLI

KW - ORIGINS

KW - EVOLUTION

KW - ALIGNMENT

KW - DNA

KW - PROTEINS

KW - TOOL

UR - http://www.scopus.com/inward/record.url?scp=85104987158&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/213298d4-a27e-3002-a4f2-d080daf678b8/

U2 - 10.3389/fmicb.2021.628622

DO - 10.3389/fmicb.2021.628622

M3 - Article

C2 - 33912145

VL - 12

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 628622

ER -