Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55
ABSTRACT 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....
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01410-22 |
| _version_ | 1811257707024351232 |
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| author | Mianzhi Wang Li Jiang Jingyi Wei Heng Zhu Junxuan Zhang Ziyi Liu Wenhui Zhang Xiaolu He Yuan Liu Ruichao Li Xia Xiao Yongxue Sun Zhenling Zeng Zhiqiang Wang |
| author_facet | Mianzhi Wang Li Jiang Jingyi Wei Heng Zhu Junxuan Zhang Ziyi Liu Wenhui Zhang Xiaolu He Yuan Liu Ruichao Li Xia Xiao Yongxue Sun Zhenling Zeng Zhiqiang Wang |
| author_sort | Mianzhi Wang |
| collection | DOAJ |
| description | ABSTRACT 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 blaCTX-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 blaCTX-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 blaCTX-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 blaCTX-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. |
| first_indexed | 2024-04-12T18:01:39Z |
| format | Article |
| id | doaj.art-99028cbf2ea4444197bb82c457656fc5 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T18:01:39Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-99028cbf2ea4444197bb82c457656fc52022-12-22T03:22:08ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.01410-22Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55Mianzhi Wang0Li Jiang1Jingyi Wei2Heng Zhu3Junxuan Zhang4Ziyi Liu5Wenhui Zhang6Xiaolu He7Yuan Liu8Ruichao Li9Xia Xiao10Yongxue Sun11Zhenling Zeng12Zhiqiang Wang13College of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaABSTRACT 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 blaCTX-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 blaCTX-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 blaCTX-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 blaCTX-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.https://journals.asm.org/doi/10.1128/spectrum.01410-22P1phage plasmidESBLsblaCTX-M-55IncYp0111 |
| spellingShingle | Mianzhi Wang Li Jiang Jingyi Wei Heng Zhu Junxuan Zhang Ziyi Liu Wenhui Zhang Xiaolu He Yuan Liu Ruichao Li Xia Xiao Yongxue Sun Zhenling Zeng Zhiqiang Wang Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 Microbiology Spectrum P1 phage plasmid ESBLs blaCTX-M-55 IncY p0111 |
| title | Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 |
| title_full | Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 |
| title_fullStr | Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 |
| title_full_unstemmed | Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 |
| title_short | Similarities of P1-Like Phage Plasmids and Their Role in the Dissemination of blaCTX-M-55 |
| title_sort | similarities of p1 like phage plasmids and their role in the dissemination of blactx m 55 |
| topic | P1 phage plasmid ESBLs blaCTX-M-55 IncY p0111 |
| url | https://journals.asm.org/doi/10.1128/spectrum.01410-22 |
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