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Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages

BACKGROUND: Shiga toxin-producing Escherichia coli O157:H7 is a foodborne pathogen that causes severe human diseases including hemolytic uremic syndrome (HUS). The virulence factor that mediates HUS, Shiga toxin (Stx), is encoded within the genome of a lambdoid prophage. Although draft sequences are...

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Autores principales: Yin, Shuang, Rusconi, Brigida, Sanjar, Fatemeh, Goswami, Kakolie, Xiaoli, Lingzi, Eppinger, Mark, Dudley, Edward G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4587872/
https://www.ncbi.nlm.nih.gov/pubmed/26416807
http://dx.doi.org/10.1186/s12864-015-1934-1
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author Yin, Shuang
Rusconi, Brigida
Sanjar, Fatemeh
Goswami, Kakolie
Xiaoli, Lingzi
Eppinger, Mark
Dudley, Edward G.
author_facet Yin, Shuang
Rusconi, Brigida
Sanjar, Fatemeh
Goswami, Kakolie
Xiaoli, Lingzi
Eppinger, Mark
Dudley, Edward G.
author_sort Yin, Shuang
collection PubMed
description BACKGROUND: Shiga toxin-producing Escherichia coli O157:H7 is a foodborne pathogen that causes severe human diseases including hemolytic uremic syndrome (HUS). The virulence factor that mediates HUS, Shiga toxin (Stx), is encoded within the genome of a lambdoid prophage. Although draft sequences are publicly available for a large number of E. coli O157:H7 strains, the high sequence similarity of stx-converting bacteriophages with other lambdoid prophages poses challenges to accurately assess the organization and plasticity among stx-converting phages due to assembly difficulties. METHODS: To further explore genome plasticity of stx-converting prophages, we enriched phage DNA from 45 ciprofloxacin-induced cultures for subsequent 454 pyrosequencing to facilitate assembly of the complete phage genomes. In total, 22 stx2a-converting phage genomes were closed. RESULTS: Comparison of the genomes distinguished nine distinct phage sequence types (PSTs) delineated by variation in obtained sequences, such as single nucleotide polymorphisms (SNPs) and insertion sequence element prevalence and location. These nine PSTs formed three distinct clusters, designated as PST1, PST2 and PST3. The PST2 cluster, identified in two clade 8 strains, was related to stx2a-converting phages previously identified in non-O157 Shiga-toxin producing E. coli (STEC) strains associated with a high incidence of HUS. The PST1 cluster contained phages related to those from E. coli O157:H7 strain Sakai (lineage I, clade 1), and PST3 contained a single phage that was distinct from the rest but most related to the phage from E. coli O157:H7 strain EC4115 (lineage I/II, clade 8). Five strains carried identical stx2a-converting phages (PST1-1) integrated at the same chromosomal locus, but these strains produced different levels of Stx2. CONCLUSION: The stx2a-converting phages of E. coli O157:H7 can be categorized into at least three phage types. Diversification within a phage type is mainly driven by IS629 and by a small number of SNPs. Polymorphisms between phage genomes may help explain differences in Stx2a production between strains, however our data indicates that genes encoded external to the phage affect toxin production as well. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1934-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-45878722015-09-30 Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages Yin, Shuang Rusconi, Brigida Sanjar, Fatemeh Goswami, Kakolie Xiaoli, Lingzi Eppinger, Mark Dudley, Edward G. BMC Genomics Research Article BACKGROUND: Shiga toxin-producing Escherichia coli O157:H7 is a foodborne pathogen that causes severe human diseases including hemolytic uremic syndrome (HUS). The virulence factor that mediates HUS, Shiga toxin (Stx), is encoded within the genome of a lambdoid prophage. Although draft sequences are publicly available for a large number of E. coli O157:H7 strains, the high sequence similarity of stx-converting bacteriophages with other lambdoid prophages poses challenges to accurately assess the organization and plasticity among stx-converting phages due to assembly difficulties. METHODS: To further explore genome plasticity of stx-converting prophages, we enriched phage DNA from 45 ciprofloxacin-induced cultures for subsequent 454 pyrosequencing to facilitate assembly of the complete phage genomes. In total, 22 stx2a-converting phage genomes were closed. RESULTS: Comparison of the genomes distinguished nine distinct phage sequence types (PSTs) delineated by variation in obtained sequences, such as single nucleotide polymorphisms (SNPs) and insertion sequence element prevalence and location. These nine PSTs formed three distinct clusters, designated as PST1, PST2 and PST3. The PST2 cluster, identified in two clade 8 strains, was related to stx2a-converting phages previously identified in non-O157 Shiga-toxin producing E. coli (STEC) strains associated with a high incidence of HUS. The PST1 cluster contained phages related to those from E. coli O157:H7 strain Sakai (lineage I, clade 1), and PST3 contained a single phage that was distinct from the rest but most related to the phage from E. coli O157:H7 strain EC4115 (lineage I/II, clade 8). Five strains carried identical stx2a-converting phages (PST1-1) integrated at the same chromosomal locus, but these strains produced different levels of Stx2. CONCLUSION: The stx2a-converting phages of E. coli O157:H7 can be categorized into at least three phage types. Diversification within a phage type is mainly driven by IS629 and by a small number of SNPs. Polymorphisms between phage genomes may help explain differences in Stx2a production between strains, however our data indicates that genes encoded external to the phage affect toxin production as well. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1934-1) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-29 /pmc/articles/PMC4587872/ /pubmed/26416807 http://dx.doi.org/10.1186/s12864-015-1934-1 Text en © Yin et al. 2015 Open AccessThis 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
Yin, Shuang
Rusconi, Brigida
Sanjar, Fatemeh
Goswami, Kakolie
Xiaoli, Lingzi
Eppinger, Mark
Dudley, Edward G.
Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title_full Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title_fullStr Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title_full_unstemmed Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title_short Escherichia coli O157:H7 strains harbor at least three distinct sequence types of Shiga toxin 2a-converting phages
title_sort escherichia coli o157:h7 strains harbor at least three distinct sequence types of shiga toxin 2a-converting phages
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4587872/
https://www.ncbi.nlm.nih.gov/pubmed/26416807
http://dx.doi.org/10.1186/s12864-015-1934-1
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