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

Abstract 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 com...

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Main Authors: Vijay K. Sharma, Suryatej Akavaram, Robert G. Schaut, Darrell O. Bayles
Format: Article
Language:English
Published: BMC 2019-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5568-6
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author Vijay K. Sharma
Suryatej Akavaram
Robert G. Schaut
Darrell O. Bayles
author_facet Vijay K. Sharma
Suryatej Akavaram
Robert G. Schaut
Darrell O. Bayles
author_sort Vijay K. Sharma
collection DOAJ
description Abstract 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.
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spelling doaj.art-120192ea47aa45a58da0e01d141800ba2022-12-22T00:45:21ZengBMCBMC Genomics1471-21642019-03-0120111810.1186/s12864-019-5568-6Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7Vijay K. Sharma0Suryatej Akavaram1Robert G. Schaut2Darrell O. Bayles3Food Safety and Enteric Pathogens Research Unit, USDA, ARS, National Animal Disease CenterFood Safety and Enteric Pathogens Research Unit, USDA, ARS, National Animal Disease CenterFood Safety and Enteric Pathogens Research Unit, USDA, ARS, National Animal Disease CenterInfectious Bacterial Diseases Research Unit, National Animal Disease Center, ARS-USDAAbstract 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.http://link.springer.com/article/10.1186/s12864-019-5568-6O157GenomicsBacteriophagesMobile elementsGenomic islandsStress response
spellingShingle Vijay K. Sharma
Suryatej Akavaram
Robert G. Schaut
Darrell O. Bayles
Comparative genomics reveals structural and functional features specific to the genome of a foodborne Escherichia coli O157:H7
BMC Genomics
O157
Genomics
Bacteriophages
Mobile elements
Genomic islands
Stress response
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 O157
Genomics
Bacteriophages
Mobile elements
Genomic islands
Stress response
url http://link.springer.com/article/10.1186/s12864-019-5568-6
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