The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica
Objectives: This study aimed to characterize the co-occurrence of the tigecycline resistance determinants tet(X4) and tmexCD2-toprJ2 in a Raoultella ornithinolytica isolate collected from a pig rectal swab at the slaughterhouse. Methods: The R. ornithinolytica isolate WS60 was subjected to antimicro...
Saved in:
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2025-05-01
|
| Series: | Journal of Global Antimicrobial Resistance |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213716525000323 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850034216309358592 |
|---|---|
| author | Weishuai Zhai Lu Liu Jijun Kang Mengjin Xiao Yiqing Wang Yao Wang Yingbo Shen Congming Wu Jianzhong Shen Yang Wang Dejun Liu |
| author_facet | Weishuai Zhai Lu Liu Jijun Kang Mengjin Xiao Yiqing Wang Yao Wang Yingbo Shen Congming Wu Jianzhong Shen Yang Wang Dejun Liu |
| author_sort | Weishuai Zhai |
| collection | DOAJ |
| description | Objectives: This study aimed to characterize the co-occurrence of the tigecycline resistance determinants tet(X4) and tmexCD2-toprJ2 in a Raoultella ornithinolytica isolate collected from a pig rectal swab at the slaughterhouse. Methods: The R. ornithinolytica isolate WS60 was subjected to antimicrobial susceptibility testing. Whole-genome sequencing (WGS) was performed to analyze the genetic features of the plasmids carrying tet(X4) and tmexCD2-toprJ2. Additionally, a conjugation assay was conducted to evaluate the transferability of these plasmids, followed by a 15-day stability test to assess the persistence of the two resistance determinants. Results: R. ornithinolytica WS60 exhibited high-level tigecycline resistance, with a minimum inhibitory concentration (MIC) of 32 μg/mL, and was also resistant to ampicillin, ampicillin-sulbactam, chloramphenicol, tetracycline, sulfamethoxazole-trimethoprim, florfenicol, and streptomycin. WGS analysis revealed that WS60 harbored three plasmids, including a 384,249-bp tmexCD2-toprJ2-carrying IncQ plasmid (pWS60–1) and a 78,159-bp tet(X4)-carrying IncFII plasmid (pWS60–2). Interestingly, pWS60–2 was identical to several plasmids found in Klebsiella spp. isolated from animals, animal-derived food, and humans. Moreover, pWS60–2 was successfully transferred to Klebsiella spp. via conjugation, whereas pWS60–1 failed to transfer. Notably, no significant fitness cost was observed in the transconjugants carrying pWS60–2. Additionally, a 15-day stability assay demonstrated that both resistance determinants were stably maintained in the bacterial population without significant loss, underscoring their persistence over time. Conclusions: This is the first report of the co-occurrence of tet(X4) and tmexCD2-toprJ2 in R. ornithinolytica. Enhanced surveillance in slaughterhouses, along with targeted interventions, should be implemented to mitigate the potential spread of mobile tigecycline resistance throughout the food production chain. |
| format | Article |
| id | doaj-art-c3feb2b6b6b64859919e3bd24b363fb5 |
| institution | DOAJ |
| issn | 2213-7165 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Global Antimicrobial Resistance |
| spelling | doaj-art-c3feb2b6b6b64859919e3bd24b363fb52025-08-20T02:57:53ZengElsevierJournal of Global Antimicrobial Resistance2213-71652025-05-014210010410.1016/j.jgar.2025.01.021The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolyticaWeishuai Zhai0Lu Liu1Jijun Kang2Mengjin Xiao3Yiqing Wang4Yao Wang5Yingbo Shen6Congming Wu7Jianzhong Shen8Yang Wang9Dejun Liu10Technology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaTechnology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China; National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; Corresponding author. Mailing address: Technology Innovation Center for Food Safety Surveillance and Detection (Hainan), Sanya Institute of China Agricultural University, Sanya, China.Objectives: This study aimed to characterize the co-occurrence of the tigecycline resistance determinants tet(X4) and tmexCD2-toprJ2 in a Raoultella ornithinolytica isolate collected from a pig rectal swab at the slaughterhouse. Methods: The R. ornithinolytica isolate WS60 was subjected to antimicrobial susceptibility testing. Whole-genome sequencing (WGS) was performed to analyze the genetic features of the plasmids carrying tet(X4) and tmexCD2-toprJ2. Additionally, a conjugation assay was conducted to evaluate the transferability of these plasmids, followed by a 15-day stability test to assess the persistence of the two resistance determinants. Results: R. ornithinolytica WS60 exhibited high-level tigecycline resistance, with a minimum inhibitory concentration (MIC) of 32 μg/mL, and was also resistant to ampicillin, ampicillin-sulbactam, chloramphenicol, tetracycline, sulfamethoxazole-trimethoprim, florfenicol, and streptomycin. WGS analysis revealed that WS60 harbored three plasmids, including a 384,249-bp tmexCD2-toprJ2-carrying IncQ plasmid (pWS60–1) and a 78,159-bp tet(X4)-carrying IncFII plasmid (pWS60–2). Interestingly, pWS60–2 was identical to several plasmids found in Klebsiella spp. isolated from animals, animal-derived food, and humans. Moreover, pWS60–2 was successfully transferred to Klebsiella spp. via conjugation, whereas pWS60–1 failed to transfer. Notably, no significant fitness cost was observed in the transconjugants carrying pWS60–2. Additionally, a 15-day stability assay demonstrated that both resistance determinants were stably maintained in the bacterial population without significant loss, underscoring their persistence over time. Conclusions: This is the first report of the co-occurrence of tet(X4) and tmexCD2-toprJ2 in R. ornithinolytica. Enhanced surveillance in slaughterhouses, along with targeted interventions, should be implemented to mitigate the potential spread of mobile tigecycline resistance throughout the food production chain.http://www.sciencedirect.com/science/article/pii/S2213716525000323tet(X4)tmexCD2-toprJ2Mobile tigecycline resistanceRaoultella ornithinolyticaHorizontal transfer |
| spellingShingle | Weishuai Zhai Lu Liu Jijun Kang Mengjin Xiao Yiqing Wang Yao Wang Yingbo Shen Congming Wu Jianzhong Shen Yang Wang Dejun Liu The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica Journal of Global Antimicrobial Resistance tet(X4) tmexCD2-toprJ2 Mobile tigecycline resistance Raoultella ornithinolytica Horizontal transfer |
| title | The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica |
| title_full | The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica |
| title_fullStr | The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica |
| title_full_unstemmed | The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica |
| title_short | The co-occurrence of tet(X4) and tmexCD2-toprJ2 mediated tigecycline resistance in Raoultella ornithinolytica |
| title_sort | co occurrence of tet x4 and tmexcd2 toprj2 mediated tigecycline resistance in raoultella ornithinolytica |
| topic | tet(X4) tmexCD2-toprJ2 Mobile tigecycline resistance Raoultella ornithinolytica Horizontal transfer |
| url | http://www.sciencedirect.com/science/article/pii/S2213716525000323 |
| work_keys_str_mv | AT weishuaizhai thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT luliu thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT jijunkang thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT mengjinxiao thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yiqingwang thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yaowang thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yingboshen thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT congmingwu thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT jianzhongshen thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yangwang thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT dejunliu thecooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT weishuaizhai cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT luliu cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT jijunkang cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT mengjinxiao cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yiqingwang cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yaowang cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yingboshen cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT congmingwu cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT jianzhongshen cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT yangwang cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica AT dejunliu cooccurrenceoftetx4andtmexcd2toprj2mediatedtigecyclineresistanceinraoultellaornithinolytica |