Cargando…

Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7

BACKGROUND: Escherichia coli O157:H7 (O157) has been linked to numerous foodborne disease outbreaks. The ability to rapidly sequence and analyze genomes is important for understanding epidemiology, virulence, survival, and evolution of outbreak strains. In the current study, we performed comparative...

Descripción completa

Detalles Bibliográficos
Autores principales: Sharma, Vijay K., Akavaram, Suryatej, Schaut, Robert G., Bayles, Darrell O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408774/
https://www.ncbi.nlm.nih.gov/pubmed/30849935
http://dx.doi.org/10.1186/s12864-019-5568-6
_version_ 1783401845824159744
author Sharma, Vijay K.
Akavaram, Suryatej
Schaut, Robert G.
Bayles, Darrell O.
author_facet Sharma, Vijay K.
Akavaram, Suryatej
Schaut, Robert G.
Bayles, Darrell O.
author_sort Sharma, Vijay K.
collection PubMed
description BACKGROUND: Escherichia coli O157:H7 (O157) has been linked to numerous foodborne disease outbreaks. The ability to rapidly sequence and analyze genomes is important for understanding epidemiology, virulence, survival, and evolution of outbreak strains. In the current study, we performed comparative genomics to determine structural and functional features of the genome of a foodborne O157 isolate NADC 6564 and infer its evolutionary relationship to other O157 strains. RESULTS: The chromosome of NADC 6564 contained 5466 kb compared to reference strains Sakai (5498 kb) and EDL933 (5547 kb) and shared 41 of its 43 Linear Conserved Blocks (LCB) with the reference strains. However, 18 of 41 LCB had inverse orientation in NADC 6564 compared to the reference strains. NADC 6564 shared 18 of 19 bacteriophages with reference strains except that the chromosomal positioning of some of the phages differed among these strains. The additional phage (P19) of NADC 6564 was located on a 39-kb insertion element (IE) encoding several hypothetical proteins, an integrase, transposases, transcriptional regulators, an adhesin, and a phosphoethanolamine transferase (PEA). The complete homologs of the 39-kb IE were found in E. coli PCN061 of porcine origin. The IE-encoded PEA showed low homology (32–33%) to four other PEA in NADC 6564 and PEA linked to mobilizable colistin resistance in E. coli but was highly homologous (95%) to a PEA of uropathogenic, avian pathogenic, and enteroaggregative E. coli. NADC 6564 showed slightly higher minimum inhibitory concentration of colistin compared to the reference strains. The 39-kb IE also contained dndBCDE and dptFGH operons encoding DNA S-modification and a restriction pathway, linked to oxidative stress tolerance and self-defense against foreign DNA, respectively. Evolutionary tree analysis grouped NADC 6564 with lineage I O157 strains. CONCLUSIONS: These results indicated that differential phage counts and different chromosomal positioning of many bacteriophages and genomic islands might have resulted in recombination events causing altered chromosomal organization in NADC 6564. Evolutionary analysis grouped NADC 6564 with lineage I strains and suggested its earlier divergence from these strains. The ability to perform S-DNA modification might affect tolerance of NADC 6564 to various stressors. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5568-6) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6408774
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-64087742019-03-21 Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7 Sharma, Vijay K. Akavaram, Suryatej Schaut, Robert G. Bayles, Darrell O. BMC Genomics Research Article BACKGROUND: Escherichia coli O157:H7 (O157) has been linked to numerous foodborne disease outbreaks. The ability to rapidly sequence and analyze genomes is important for understanding epidemiology, virulence, survival, and evolution of outbreak strains. In the current study, we performed comparative genomics to determine structural and functional features of the genome of a foodborne O157 isolate NADC 6564 and infer its evolutionary relationship to other O157 strains. RESULTS: The chromosome of NADC 6564 contained 5466 kb compared to reference strains Sakai (5498 kb) and EDL933 (5547 kb) and shared 41 of its 43 Linear Conserved Blocks (LCB) with the reference strains. However, 18 of 41 LCB had inverse orientation in NADC 6564 compared to the reference strains. NADC 6564 shared 18 of 19 bacteriophages with reference strains except that the chromosomal positioning of some of the phages differed among these strains. The additional phage (P19) of NADC 6564 was located on a 39-kb insertion element (IE) encoding several hypothetical proteins, an integrase, transposases, transcriptional regulators, an adhesin, and a phosphoethanolamine transferase (PEA). The complete homologs of the 39-kb IE were found in E. coli PCN061 of porcine origin. The IE-encoded PEA showed low homology (32–33%) to four other PEA in NADC 6564 and PEA linked to mobilizable colistin resistance in E. coli but was highly homologous (95%) to a PEA of uropathogenic, avian pathogenic, and enteroaggregative E. coli. NADC 6564 showed slightly higher minimum inhibitory concentration of colistin compared to the reference strains. The 39-kb IE also contained dndBCDE and dptFGH operons encoding DNA S-modification and a restriction pathway, linked to oxidative stress tolerance and self-defense against foreign DNA, respectively. Evolutionary tree analysis grouped NADC 6564 with lineage I O157 strains. CONCLUSIONS: These results indicated that differential phage counts and different chromosomal positioning of many bacteriophages and genomic islands might have resulted in recombination events causing altered chromosomal organization in NADC 6564. Evolutionary analysis grouped NADC 6564 with lineage I strains and suggested its earlier divergence from these strains. The ability to perform S-DNA modification might affect tolerance of NADC 6564 to various stressors. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5568-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-08 /pmc/articles/PMC6408774/ /pubmed/30849935 http://dx.doi.org/10.1186/s12864-019-5568-6 Text en © The Author(s). 2019 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
Sharma, Vijay K.
Akavaram, Suryatej
Schaut, Robert G.
Bayles, Darrell O.
Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title_full Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title_fullStr Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title_full_unstemmed Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title_short Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
title_sort comparative genomics reveals structural and functional features specific to the genome of a foodborne escherichia coli o157:h7
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408774/
https://www.ncbi.nlm.nih.gov/pubmed/30849935
http://dx.doi.org/10.1186/s12864-019-5568-6
work_keys_str_mv AT sharmavijayk comparativegenomicsrevealsstructuralandfunctionalfeaturesspecifictothegenomeofafoodborneescherichiacolio157h7
AT akavaramsuryatej comparativegenomicsrevealsstructuralandfunctionalfeaturesspecifictothegenomeofafoodborneescherichiacolio157h7
AT schautrobertg comparativegenomicsrevealsstructuralandfunctionalfeaturesspecifictothegenomeofafoodborneescherichiacolio157h7
AT baylesdarrello comparativegenomicsrevealsstructuralandfunctionalfeaturesspecifictothegenomeofafoodborneescherichiacolio157h7