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Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics

In recent years, bla(CTX-M-55)-positive Escherichia coli has been widely reported in multiple locations with an increasing trend in prevalence, yet few studies have comprehensively analyzed the transmission characteristics and epidemiological patterns of bla(CTX-M-55)-positive E. coli. Here, we cons...

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Autores principales: Yang, Jin-Tao, Zhang, Li-Juan, Lu, Yang, Zhang, Rong-Min, Jiang, Hong-Xia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434037/
https://www.ncbi.nlm.nih.gov/pubmed/37358409
http://dx.doi.org/10.1128/spectrum.01089-23
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author Yang, Jin-Tao
Zhang, Li-Juan
Lu, Yang
Zhang, Rong-Min
Jiang, Hong-Xia
author_facet Yang, Jin-Tao
Zhang, Li-Juan
Lu, Yang
Zhang, Rong-Min
Jiang, Hong-Xia
author_sort Yang, Jin-Tao
collection PubMed
description In recent years, bla(CTX-M-55)-positive Escherichia coli has been widely reported in multiple locations with an increasing trend in prevalence, yet few studies have comprehensively analyzed the transmission characteristics and epidemiological patterns of bla(CTX-M-55)-positive E. coli. Here, we constructed a bla(CTX-M-55)-positive E. coli global genomic data set as completely as possible and explored the epidemiology and potential impact of bla(CTX-M-55)-positive E. coli on a global scale by high-resolution bioinformatics methods. The results show that bla(CTX-M-55)-positive E. coli has spread widely worldwide, especially in Asia, with the rich sequence typing (ST) diversity and high proportion of auxiliary genome occupancy indicating a high degree of openness. The phylogenetic tree suggests that bla(CTX-M-55)-positive E. coli is frequently clonally transmitted between the three human-animal environments and often cotransmitted with fosA, mcr, bla(NDM), and tet(X). The stable presence of InclI1 and InclI2 in different hosts from different sources suggests that this part of the plasmid drives the widespread transmission of bla(CTX-M-55)-positive E. coli. We inductively clustered all bla(CTX-M-55) flanking environmental gene structures and obtained five types. Notably, “ISEcp1-bla(CTX-M-55)-orf477-(Tn2)” and “IS26(IS15DI)-hp-hp-bla(CTX-M-55)-orf477-hp-bla(TEM)-IS26-hp-IS26-Tn2” are dominant in “humans” and in “animals and related foods,” respectively. Overall, our findings highlight the importance of whole-genome sequencing-based surveillance in exploring the transmission and evolution of bla(CTX-M-55)-positive E. coli in the context of “One Health,” and they serve as a reminder to strengthen the surveillance of bla(CTX-M-55)-positive E. coli in order to address the potential risk of future large outbreaks. IMPORTANCE CTX-M-55 was first discovered in Thailand in 2004, and today, this enzyme is the most common CTX-M subtype in E. coli of animal origin in China. Thus, bla(CTX-M-55)-positive E. coli getting widely spread is a growing public health problem. Although prevalence surveys of bla(CTX-M-55)-positive E. coli in different hosts have been widely reported in recent years, they remain insufficient in “One Health” context and from a global comprehensive perspective. Here, we constructed a genomic database of 2144 bla(CTX-M-55)-positive E. coli and used bioinformatics methods to resolve the spread and evolution of bla(CTX-M-55)-positive E. coli. The results suggest a potential risk of rapid transmission of bla(CTX-M-55)-positive E. coli and that long-term continuous surveillance of bla(CTX-M-55)-positive E. coli should be emphasized.
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spelling pubmed-104340372023-08-18 Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics Yang, Jin-Tao Zhang, Li-Juan Lu, Yang Zhang, Rong-Min Jiang, Hong-Xia Microbiol Spectr Research Article In recent years, bla(CTX-M-55)-positive Escherichia coli has been widely reported in multiple locations with an increasing trend in prevalence, yet few studies have comprehensively analyzed the transmission characteristics and epidemiological patterns of bla(CTX-M-55)-positive E. coli. Here, we constructed a bla(CTX-M-55)-positive E. coli global genomic data set as completely as possible and explored the epidemiology and potential impact of bla(CTX-M-55)-positive E. coli on a global scale by high-resolution bioinformatics methods. The results show that bla(CTX-M-55)-positive E. coli has spread widely worldwide, especially in Asia, with the rich sequence typing (ST) diversity and high proportion of auxiliary genome occupancy indicating a high degree of openness. The phylogenetic tree suggests that bla(CTX-M-55)-positive E. coli is frequently clonally transmitted between the three human-animal environments and often cotransmitted with fosA, mcr, bla(NDM), and tet(X). The stable presence of InclI1 and InclI2 in different hosts from different sources suggests that this part of the plasmid drives the widespread transmission of bla(CTX-M-55)-positive E. coli. We inductively clustered all bla(CTX-M-55) flanking environmental gene structures and obtained five types. Notably, “ISEcp1-bla(CTX-M-55)-orf477-(Tn2)” and “IS26(IS15DI)-hp-hp-bla(CTX-M-55)-orf477-hp-bla(TEM)-IS26-hp-IS26-Tn2” are dominant in “humans” and in “animals and related foods,” respectively. Overall, our findings highlight the importance of whole-genome sequencing-based surveillance in exploring the transmission and evolution of bla(CTX-M-55)-positive E. coli in the context of “One Health,” and they serve as a reminder to strengthen the surveillance of bla(CTX-M-55)-positive E. coli in order to address the potential risk of future large outbreaks. IMPORTANCE CTX-M-55 was first discovered in Thailand in 2004, and today, this enzyme is the most common CTX-M subtype in E. coli of animal origin in China. Thus, bla(CTX-M-55)-positive E. coli getting widely spread is a growing public health problem. Although prevalence surveys of bla(CTX-M-55)-positive E. coli in different hosts have been widely reported in recent years, they remain insufficient in “One Health” context and from a global comprehensive perspective. Here, we constructed a genomic database of 2144 bla(CTX-M-55)-positive E. coli and used bioinformatics methods to resolve the spread and evolution of bla(CTX-M-55)-positive E. coli. The results suggest a potential risk of rapid transmission of bla(CTX-M-55)-positive E. coli and that long-term continuous surveillance of bla(CTX-M-55)-positive E. coli should be emphasized. American Society for Microbiology 2023-06-26 /pmc/articles/PMC10434037/ /pubmed/37358409 http://dx.doi.org/10.1128/spectrum.01089-23 Text en Copyright © 2023 Yang 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
Yang, Jin-Tao
Zhang, Li-Juan
Lu, Yang
Zhang, Rong-Min
Jiang, Hong-Xia
Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title_full Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title_fullStr Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title_full_unstemmed Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title_short Genomic Insights into Global bla(CTX-M-55)-Positive Escherichia coli Epidemiology and Transmission Characteristics
title_sort genomic insights into global bla(ctx-m-55)-positive escherichia coli epidemiology and transmission characteristics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434037/
https://www.ncbi.nlm.nih.gov/pubmed/37358409
http://dx.doi.org/10.1128/spectrum.01089-23
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