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Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)

The P1-like phage plasmid (PP) has been widely used as a molecular biology tool, but its role as an active accessory cargo element is not fully understood. In this study, we provide insights into the structural features and gene content similarities of 77 P1-like PPs in the RefSeq database. We also...

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Autores principales: Wang, Mianzhi, Jiang, Li, Wei, Jingyi, Zhu, Heng, Zhang, Junxuan, Liu, Ziyi, Zhang, Wenhui, He, Xiaolu, Liu, Yuan, Li, Ruichao, Xiao, Xia, Sun, Yongxue, Zeng, Zhenling, Wang, Zhiqiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9603915/
https://www.ncbi.nlm.nih.gov/pubmed/36069562
http://dx.doi.org/10.1128/spectrum.01410-22
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author Wang, Mianzhi
Jiang, Li
Wei, Jingyi
Zhu, Heng
Zhang, Junxuan
Liu, Ziyi
Zhang, Wenhui
He, Xiaolu
Liu, Yuan
Li, Ruichao
Xiao, Xia
Sun, Yongxue
Zeng, Zhenling
Wang, Zhiqiang
author_facet Wang, Mianzhi
Jiang, Li
Wei, Jingyi
Zhu, Heng
Zhang, Junxuan
Liu, Ziyi
Zhang, Wenhui
He, Xiaolu
Liu, Yuan
Li, Ruichao
Xiao, Xia
Sun, Yongxue
Zeng, Zhenling
Wang, Zhiqiang
author_sort Wang, Mianzhi
collection PubMed
description The P1-like phage plasmid (PP) has been widely used as a molecular biology tool, but its role as an active accessory cargo element is not fully understood. In this study, we provide insights into the structural features and gene content similarities of 77 P1-like PPs in the RefSeq database. We also describe a P1-like PP carrying a bla(CTX-M-55) gene, JL22, which was isolated from a clinical strain of Escherichia coli from a duck farm. P1-like PPs were very similar and conserved based on gene content similarities, with only eight highly variable regions. Importantly, two kinds of replicon types, namely, IncY and p0111, were identified and can be used to specifically identify the P1-like phage. JL22 is similar to P1, acquiring an important foreign DNA fragment with two obvious features, namely, the plasmid replication gene repA′ (p0111) replacing the gene repA (IncY) and a 4,200-bp fragment mobilized by IS1380 and IS5 and containing a bla(CTX-M-55) gene and a trpB gene encoding tryptophan synthase (indole salvaging). The JL22 phage could be induced but had no lytic capacities. However, a lysogenic recipient and intact structure of JL22 virions were observed, showing that the extended-spectrum β-lactamase bla(CTX-M-55) gene was successfully transferred. Overall, conserved genes can be a good complement to improve the identification efficiency and accuracy in future screening for P1-like PPs. Moreover, the highly conserved structures may be important for their prevalence and dissemination. IMPORTANCE As a PP, P1 DNA exists as a low-copy-number plasmid and replicates autonomously with a lysogenization style. This unique mode of P1-like elements probably indicates a stable contribution to antibiotic resistance. After analyzing these elements, we show that P1-like PPs are very similar and conserved, with only eight highly variable regions. Moreover, we observed the occurrence of replicon IncY and p0111 only in the P1-like PP community, implying that these conserved regions, coupled with IncY and p0111, can be an important complement in future screening of P1-like PPs. Identification and characterization of JL22 confirmed our findings that major changes were located in variable regions, including the first detection of bla(CTX-M-55) in such a mobile genetic element. This suggests that these variable regions may facilitate foreign DNA mobilization. This study features a comprehensive genetic analysis of P1-like PPs, providing new insights into the dissemination mechanisms of antibiotic resistance through P1 PPs.
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spelling pubmed-96039152022-10-27 Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55) Wang, Mianzhi Jiang, Li Wei, Jingyi Zhu, Heng Zhang, Junxuan Liu, Ziyi Zhang, Wenhui He, Xiaolu Liu, Yuan Li, Ruichao Xiao, Xia Sun, Yongxue Zeng, Zhenling Wang, Zhiqiang Microbiol Spectr Research Article The P1-like phage plasmid (PP) has been widely used as a molecular biology tool, but its role as an active accessory cargo element is not fully understood. In this study, we provide insights into the structural features and gene content similarities of 77 P1-like PPs in the RefSeq database. We also describe a P1-like PP carrying a bla(CTX-M-55) gene, JL22, which was isolated from a clinical strain of Escherichia coli from a duck farm. P1-like PPs were very similar and conserved based on gene content similarities, with only eight highly variable regions. Importantly, two kinds of replicon types, namely, IncY and p0111, were identified and can be used to specifically identify the P1-like phage. JL22 is similar to P1, acquiring an important foreign DNA fragment with two obvious features, namely, the plasmid replication gene repA′ (p0111) replacing the gene repA (IncY) and a 4,200-bp fragment mobilized by IS1380 and IS5 and containing a bla(CTX-M-55) gene and a trpB gene encoding tryptophan synthase (indole salvaging). The JL22 phage could be induced but had no lytic capacities. However, a lysogenic recipient and intact structure of JL22 virions were observed, showing that the extended-spectrum β-lactamase bla(CTX-M-55) gene was successfully transferred. Overall, conserved genes can be a good complement to improve the identification efficiency and accuracy in future screening for P1-like PPs. Moreover, the highly conserved structures may be important for their prevalence and dissemination. IMPORTANCE As a PP, P1 DNA exists as a low-copy-number plasmid and replicates autonomously with a lysogenization style. This unique mode of P1-like elements probably indicates a stable contribution to antibiotic resistance. After analyzing these elements, we show that P1-like PPs are very similar and conserved, with only eight highly variable regions. Moreover, we observed the occurrence of replicon IncY and p0111 only in the P1-like PP community, implying that these conserved regions, coupled with IncY and p0111, can be an important complement in future screening of P1-like PPs. Identification and characterization of JL22 confirmed our findings that major changes were located in variable regions, including the first detection of bla(CTX-M-55) in such a mobile genetic element. This suggests that these variable regions may facilitate foreign DNA mobilization. This study features a comprehensive genetic analysis of P1-like PPs, providing new insights into the dissemination mechanisms of antibiotic resistance through P1 PPs. American Society for Microbiology 2022-09-07 /pmc/articles/PMC9603915/ /pubmed/36069562 http://dx.doi.org/10.1128/spectrum.01410-22 Text en Copyright © 2022 Wang 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
Wang, Mianzhi
Jiang, Li
Wei, Jingyi
Zhu, Heng
Zhang, Junxuan
Liu, Ziyi
Zhang, Wenhui
He, Xiaolu
Liu, Yuan
Li, Ruichao
Xiao, Xia
Sun, Yongxue
Zeng, Zhenling
Wang, Zhiqiang
Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title_full Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title_fullStr Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title_full_unstemmed Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title_short Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of bla(CTX-M-55)
title_sort similarities of p1-like phage plasmids and their role in the dissemination of bla(ctx-m-55)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9603915/
https://www.ncbi.nlm.nih.gov/pubmed/36069562
http://dx.doi.org/10.1128/spectrum.01410-22
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