Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin
ABSTRACT The emergence of the plasmid-mediated high levels of the tigecycline resistance gene has drawn worldwide attention and has posed a major threat to public health. In this study, we investigated the prevalence of the tet(X4)-positive Enterobacterales isolates collected from a pig slaughterhou...
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| Format: | Article |
| Language: | English |
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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.01615-22 |
| _version_ | 1811198163420184576 |
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| author | Qin Wang Changwei Lei Hansen Cheng Xue Yang Zheren Huang Xuan Chen Zijing Ju Haoyu Zhang Hongning Wang |
| author_facet | Qin Wang Changwei Lei Hansen Cheng Xue Yang Zheren Huang Xuan Chen Zijing Ju Haoyu Zhang Hongning Wang |
| author_sort | Qin Wang |
| collection | DOAJ |
| description | ABSTRACT The emergence of the plasmid-mediated high levels of the tigecycline resistance gene has drawn worldwide attention and has posed a major threat to public health. In this study, we investigated the prevalence of the tet(X4)-positive Enterobacterales isolates collected from a pig slaughterhouse and farms. A total of 101 tigecycline resistance strains were isolated from 353 samples via a medium with tigecycline, of which 33 carried tet(X4) (9.35%, 33/353) and 2 carried tet(X6) (0.57%, 2/353). These strains belong to seven different species, with Escherichia coli being the main host bacteria. Importantly, this report is the first one to demonstrate that tet(X4) was observed in Morganella morganii. Whole-genome sequencing results revealed that tet(X4)-positive bacteria can coexist with other resistance genes, such as blaNDM-1 and cfr. Additionally, we were the first to report that tet(X4) and blaNDM-1 coexist in a Klebsiella quasipneumoniae strain. The phylogenetic tree of 533 tet(X4)-positive E. coli strains was constructed using 509 strains from the NCBI genome assembly database and 24 strains from this study, which arose from 8 sources and belonged to 135 sequence types (STs) worldwide. We used Nanopore sequencing to interpret the selected 21 nonclonal and representative strains and observed that 19 tet(X4)-harboring plasmids were classified into 8 replicon types, and 2 tet(X6) genes were located on integrating conjugative elements. A total of 68.42% of plasmids carrying tet(X4) were transferred successfully with a conjugation frequency of 10−2 to 10−7. These findings highlight that diverse plasmids drive the widespread dissemination of the tigecycline resistance gene tet(X4) in Enterobacterales of porcine origin. IMPORTANCE Tigecycline is considered to be the last resort of defense against diseases caused by broad-spectrum resistant Gram-negative bacteria. In this study, we systematically analyzed the prevalence and genetic environments of the resistance gene tet(X4) in a pig slaughterhouse and farms and the evolutionary relationship of 533 tet(X4)-positive Escherichia coli strains, including 509 tet(X4)-positive E. coli strains selected from the 27,802 assembled genomes of E. coli from the NCBI between 2002 and 2022. The drug resistance of tigecycline is widely prevalent in pig farms where tetracycline is used as a veterinary drug. This prevalence suggests that pigs are a large reservoir of tet(X4) and that tet(X4) can spread horizontally through the food chain via mobile genetic elements. Furthermore, tetracycline resistance may drive tigecycline resistance through some mechanisms. Therefore, it is important to monitor tigecycline resistance, develop effective control measures, and focus on tetracycline use in the pig farms. |
| first_indexed | 2024-04-12T01:26:12Z |
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| id | doaj.art-3c212327420e4ec7b0d1e4b6bd2e9311 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T01:26:12Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj.art-3c212327420e4ec7b0d1e4b6bd2e93112022-12-22T03:53:38ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.01615-22Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine OriginQin Wang0Changwei Lei1Hansen Cheng2Xue Yang3Zheren Huang4Xuan Chen5Zijing Ju6Haoyu Zhang7Hongning Wang8Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan Province, People’s Republic of ChinaABSTRACT The emergence of the plasmid-mediated high levels of the tigecycline resistance gene has drawn worldwide attention and has posed a major threat to public health. In this study, we investigated the prevalence of the tet(X4)-positive Enterobacterales isolates collected from a pig slaughterhouse and farms. A total of 101 tigecycline resistance strains were isolated from 353 samples via a medium with tigecycline, of which 33 carried tet(X4) (9.35%, 33/353) and 2 carried tet(X6) (0.57%, 2/353). These strains belong to seven different species, with Escherichia coli being the main host bacteria. Importantly, this report is the first one to demonstrate that tet(X4) was observed in Morganella morganii. Whole-genome sequencing results revealed that tet(X4)-positive bacteria can coexist with other resistance genes, such as blaNDM-1 and cfr. Additionally, we were the first to report that tet(X4) and blaNDM-1 coexist in a Klebsiella quasipneumoniae strain. The phylogenetic tree of 533 tet(X4)-positive E. coli strains was constructed using 509 strains from the NCBI genome assembly database and 24 strains from this study, which arose from 8 sources and belonged to 135 sequence types (STs) worldwide. We used Nanopore sequencing to interpret the selected 21 nonclonal and representative strains and observed that 19 tet(X4)-harboring plasmids were classified into 8 replicon types, and 2 tet(X6) genes were located on integrating conjugative elements. A total of 68.42% of plasmids carrying tet(X4) were transferred successfully with a conjugation frequency of 10−2 to 10−7. These findings highlight that diverse plasmids drive the widespread dissemination of the tigecycline resistance gene tet(X4) in Enterobacterales of porcine origin. IMPORTANCE Tigecycline is considered to be the last resort of defense against diseases caused by broad-spectrum resistant Gram-negative bacteria. In this study, we systematically analyzed the prevalence and genetic environments of the resistance gene tet(X4) in a pig slaughterhouse and farms and the evolutionary relationship of 533 tet(X4)-positive Escherichia coli strains, including 509 tet(X4)-positive E. coli strains selected from the 27,802 assembled genomes of E. coli from the NCBI between 2002 and 2022. The drug resistance of tigecycline is widely prevalent in pig farms where tetracycline is used as a veterinary drug. This prevalence suggests that pigs are a large reservoir of tet(X4) and that tet(X4) can spread horizontally through the food chain via mobile genetic elements. Furthermore, tetracycline resistance may drive tigecycline resistance through some mechanisms. Therefore, it is important to monitor tigecycline resistance, develop effective control measures, and focus on tetracycline use in the pig farms.https://journals.asm.org/doi/10.1128/spectrum.01615-22Enterobacteralestigecycline resistancetet(X4)evolutionary relationshipgenetic environments |
| spellingShingle | Qin Wang Changwei Lei Hansen Cheng Xue Yang Zheren Huang Xuan Chen Zijing Ju Haoyu Zhang Hongning Wang Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin Microbiology Spectrum Enterobacterales tigecycline resistance tet(X4) evolutionary relationship genetic environments |
| title | Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin |
| title_full | Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin |
| title_fullStr | Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin |
| title_full_unstemmed | Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin |
| title_short | Widespread Dissemination of Plasmid-Mediated Tigecycline Resistance Gene tet(X4) in Enterobacterales of Porcine Origin |
| title_sort | widespread dissemination of plasmid mediated tigecycline resistance gene tet x4 in enterobacterales of porcine origin |
| topic | Enterobacterales tigecycline resistance tet(X4) evolutionary relationship genetic environments |
| url | https://journals.asm.org/doi/10.1128/spectrum.01615-22 |
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