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An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127

Uropathogenic Escherichia coli (UPEC) is one of the most common causes of urinary tract infections. Here, we report for the first time the whole-genome sequencing (WGS) and analysis of four extended-spectrum β-lactamase (ESBL), UPEC sequence type (ST) 127 isolates that were recovered from patients i...

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Autores principales: Cave, Rory, Ter-Stepanyan, Mary M., Kotsinyan, Nune, Mkrtchyan, Hermine V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769692/
https://www.ncbi.nlm.nih.gov/pubmed/36416548
http://dx.doi.org/10.1128/spectrum.02511-22
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author Cave, Rory
Ter-Stepanyan, Mary M.
Kotsinyan, Nune
Mkrtchyan, Hermine V.
author_facet Cave, Rory
Ter-Stepanyan, Mary M.
Kotsinyan, Nune
Mkrtchyan, Hermine V.
author_sort Cave, Rory
collection PubMed
description Uropathogenic Escherichia coli (UPEC) is one of the most common causes of urinary tract infections. Here, we report for the first time the whole-genome sequencing (WGS) and analysis of four extended-spectrum β-lactamase (ESBL), UPEC sequence type (ST) 127 isolates that were recovered from patients in five hospitals in Armenia from January to August of 2019. A phylogenetic comparison revealed that our isolates were closely related to each other by their core and accessory genomes, despite having been isolated from different regions and hospitals in Armenia. We identified unique genes in our isolates and in a closely related isolate recovered in France. The unique genes (hemolysin E virulence gene, lactate utilization operon lutABC, and endonuclease restriction modification operon hsdMSR) were identified in three separate genomic regions that were adjacent to prophage genes, including one region containing the TonB-dependent iron siderophore receptor gene ireA, which was only found in 5 other ST127 isolates from the European Nucleotide Archive (ENA). We further identified that these isolates possessed unique virulence and metabolic genes and harbored antibiotic resistance genes, including the ESBL genes bla(CTX-M-3) (n = 3), bla(CTX-M-236) (n = 1), and bla(TEM-1) (n = 1), in addition to a quinolone resistance protein gene qnrD1 (n = 1), which was absent in the ST127 isolates obtained from the ENA. Moreover, a plasmid replicon gene IncI2 (n = 1) was unique to ARM88 of the Armenian isolates. Our findings demonstrate that at the time of this study, E. coli ST127 was a cause of urinary tract infections in patients in different regions of Armenia, with a possibility of cross-country transmission between Armenia and France. IMPORTANCE Whole-genome sequencing studies of pathogens causing infectious diseases are seriously lacking in Armenia, hampering global efforts to track, trace and contain infectious disease outbreaks. In this study, we report for the first-time the whole-genome sequencing and analysis of ESBL UPEC ST127 isolates recovered from hospitalized patients in Armenia and compare them with other E. coli ST127 retrieved from the ENA. We found close genetic similarities of the Armenian isolates, indicating that E. coli ST127 was potentially a dominant lineage causing urinary tract infections in Armenia. Furthermore, we identified unique genes that were horizontally acquired in the clusters of Armenian and French isolates that were absent in other ST127 isolates obtained from the ENA. Our findings highlight a possible cross-country transmission between Armenia and France and the idea that the implementation of WGS surveillance could contribute to global efforts in tackling antibiotic resistance, as bacteria carrying antimicrobial resistance (AMR) genes do not recognize borders.
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spelling pubmed-97696922022-12-22 An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127 Cave, Rory Ter-Stepanyan, Mary M. Kotsinyan, Nune Mkrtchyan, Hermine V. Microbiol Spectr Research Article Uropathogenic Escherichia coli (UPEC) is one of the most common causes of urinary tract infections. Here, we report for the first time the whole-genome sequencing (WGS) and analysis of four extended-spectrum β-lactamase (ESBL), UPEC sequence type (ST) 127 isolates that were recovered from patients in five hospitals in Armenia from January to August of 2019. A phylogenetic comparison revealed that our isolates were closely related to each other by their core and accessory genomes, despite having been isolated from different regions and hospitals in Armenia. We identified unique genes in our isolates and in a closely related isolate recovered in France. The unique genes (hemolysin E virulence gene, lactate utilization operon lutABC, and endonuclease restriction modification operon hsdMSR) were identified in three separate genomic regions that were adjacent to prophage genes, including one region containing the TonB-dependent iron siderophore receptor gene ireA, which was only found in 5 other ST127 isolates from the European Nucleotide Archive (ENA). We further identified that these isolates possessed unique virulence and metabolic genes and harbored antibiotic resistance genes, including the ESBL genes bla(CTX-M-3) (n = 3), bla(CTX-M-236) (n = 1), and bla(TEM-1) (n = 1), in addition to a quinolone resistance protein gene qnrD1 (n = 1), which was absent in the ST127 isolates obtained from the ENA. Moreover, a plasmid replicon gene IncI2 (n = 1) was unique to ARM88 of the Armenian isolates. Our findings demonstrate that at the time of this study, E. coli ST127 was a cause of urinary tract infections in patients in different regions of Armenia, with a possibility of cross-country transmission between Armenia and France. IMPORTANCE Whole-genome sequencing studies of pathogens causing infectious diseases are seriously lacking in Armenia, hampering global efforts to track, trace and contain infectious disease outbreaks. In this study, we report for the first-time the whole-genome sequencing and analysis of ESBL UPEC ST127 isolates recovered from hospitalized patients in Armenia and compare them with other E. coli ST127 retrieved from the ENA. We found close genetic similarities of the Armenian isolates, indicating that E. coli ST127 was potentially a dominant lineage causing urinary tract infections in Armenia. Furthermore, we identified unique genes that were horizontally acquired in the clusters of Armenian and French isolates that were absent in other ST127 isolates obtained from the ENA. Our findings highlight a possible cross-country transmission between Armenia and France and the idea that the implementation of WGS surveillance could contribute to global efforts in tackling antibiotic resistance, as bacteria carrying antimicrobial resistance (AMR) genes do not recognize borders. American Society for Microbiology 2022-11-23 /pmc/articles/PMC9769692/ /pubmed/36416548 http://dx.doi.org/10.1128/spectrum.02511-22 Text en Copyright © 2022 Cave et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Cave, Rory
Ter-Stepanyan, Mary M.
Kotsinyan, Nune
Mkrtchyan, Hermine V.
An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title_full An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title_fullStr An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title_full_unstemmed An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title_short An Emerging Lineage of Uropathogenic Extended Spectrum β-Lactamase Escherichia coli ST127
title_sort emerging lineage of uropathogenic extended spectrum β-lactamase escherichia coli st127
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769692/
https://www.ncbi.nlm.nih.gov/pubmed/36416548
http://dx.doi.org/10.1128/spectrum.02511-22
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