Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid
The prevalence of plasmid-mediated tigecycline resistance gene tet(X4) is presenting an increasing trend. Once tet(X4)-bearing plasmids are captured by multidrug-resistant bacteria, such as blaNDM and mcr-coharboring bacteria, it will promote bacteria to develop an ultra-broad resistance spectrum, l...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-10-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1010387/full |
| _version_ | 1811237198599553024 |
|---|---|
| author | Xia Xiao Xia Xiao Ziyi Liu Ziyi Liu Xiaojun Chen Xiaojun Chen Kai Peng Kai Peng Ruichao Li Ruichao Li Ruichao Li Yuan Liu Yuan Liu Yuan Liu Zhiqiang Wang Zhiqiang Wang |
| author_facet | Xia Xiao Xia Xiao Ziyi Liu Ziyi Liu Xiaojun Chen Xiaojun Chen Kai Peng Kai Peng Ruichao Li Ruichao Li Ruichao Li Yuan Liu Yuan Liu Yuan Liu Zhiqiang Wang Zhiqiang Wang |
| author_sort | Xia Xiao |
| collection | DOAJ |
| description | The prevalence of plasmid-mediated tigecycline resistance gene tet(X4) is presenting an increasing trend. Once tet(X4)-bearing plasmids are captured by multidrug-resistant bacteria, such as blaNDM and mcr-coharboring bacteria, it will promote bacteria to develop an ultra-broad resistance spectrum, limiting clinical treatment options. However, little is known about the destiny of such bacteria or how they will evolve in the future. Herein, we constructed a multidrug-resistant bacteria coharboring tet(X4), blaNDM-5, and mcr-1 by introducing a tet(X4)-bearing plasmid into a blaNDM-5 and mcr-1 positive E. coli strain. Subsequently, the stability of tet(X4) and the plasmid was measured after being evolved under tigecycline or antibiotic-free circumstance. Interestingly, we observed both tet(X4)-bearing plasmids in tigecycline treated strains and non-tigecycline treated strains were stable, which might be jointly affected by the increased conjugation frequency and the structural alterations of the tet(X4)-positive plasmid. However, the stability of tet(X4) gene showed different scenarios in the two types of evolved strains. The tet(X4) gene in non-tigecycline treated strains was stable whereas the tet(X4) gene was discarded rapidly in tigecycline treated strains. Accordingly, we found the expression levels of tet(X4) gene in tigecycline-treated strains were several times higher than in non-tigecycline treated strains and ancestral strains, which might in turn impose a stronger burden on the host bacteria. SNPs analysis revealed that a myriad of mutations occurred in genes involving in conjugation transfer, and the missense mutation of marR gene in chromosome of tigecycline treated strains might account for the completely different stability of tet(X4)-bearing plasmid and tet(X4) gene. Collectively, these findings shed a light on the possibility of the emergence of multidrug resistant bacteria due to the transmission of tet(X4)-bearing plasmid, and highlighted that the antibiotic residues may be critical to the development of such bacteria. |
| first_indexed | 2024-04-12T12:21:56Z |
| format | Article |
| id | doaj.art-337dd18f175546c4bf27f2bcc12e14ad |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-12T12:21:56Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-337dd18f175546c4bf27f2bcc12e14ad2022-12-22T03:33:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-10-011310.3389/fmicb.2022.10103871010387Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmidXia Xiao0Xia Xiao1Ziyi Liu2Ziyi Liu3Xiaojun Chen4Xiaojun Chen5Kai Peng6Kai Peng7Ruichao Li8Ruichao Li9Ruichao Li10Yuan Liu11Yuan Liu12Yuan Liu13Zhiqiang Wang14Zhiqiang Wang15College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaInstitute of Comparative Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaInstitute of Comparative Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, ChinaThe prevalence of plasmid-mediated tigecycline resistance gene tet(X4) is presenting an increasing trend. Once tet(X4)-bearing plasmids are captured by multidrug-resistant bacteria, such as blaNDM and mcr-coharboring bacteria, it will promote bacteria to develop an ultra-broad resistance spectrum, limiting clinical treatment options. However, little is known about the destiny of such bacteria or how they will evolve in the future. Herein, we constructed a multidrug-resistant bacteria coharboring tet(X4), blaNDM-5, and mcr-1 by introducing a tet(X4)-bearing plasmid into a blaNDM-5 and mcr-1 positive E. coli strain. Subsequently, the stability of tet(X4) and the plasmid was measured after being evolved under tigecycline or antibiotic-free circumstance. Interestingly, we observed both tet(X4)-bearing plasmids in tigecycline treated strains and non-tigecycline treated strains were stable, which might be jointly affected by the increased conjugation frequency and the structural alterations of the tet(X4)-positive plasmid. However, the stability of tet(X4) gene showed different scenarios in the two types of evolved strains. The tet(X4) gene in non-tigecycline treated strains was stable whereas the tet(X4) gene was discarded rapidly in tigecycline treated strains. Accordingly, we found the expression levels of tet(X4) gene in tigecycline-treated strains were several times higher than in non-tigecycline treated strains and ancestral strains, which might in turn impose a stronger burden on the host bacteria. SNPs analysis revealed that a myriad of mutations occurred in genes involving in conjugation transfer, and the missense mutation of marR gene in chromosome of tigecycline treated strains might account for the completely different stability of tet(X4)-bearing plasmid and tet(X4) gene. Collectively, these findings shed a light on the possibility of the emergence of multidrug resistant bacteria due to the transmission of tet(X4)-bearing plasmid, and highlighted that the antibiotic residues may be critical to the development of such bacteria.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1010387/fullblaNDM-5mcr-1tet(X4)-bearing plasmidplasmid stabilitytet(X4) stability |
| spellingShingle | Xia Xiao Xia Xiao Ziyi Liu Ziyi Liu Xiaojun Chen Xiaojun Chen Kai Peng Kai Peng Ruichao Li Ruichao Li Ruichao Li Yuan Liu Yuan Liu Yuan Liu Zhiqiang Wang Zhiqiang Wang Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid Frontiers in Microbiology blaNDM-5 mcr-1 tet(X4)-bearing plasmid plasmid stability tet(X4) stability |
| title | Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid |
| title_full | Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid |
| title_fullStr | Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid |
| title_full_unstemmed | Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid |
| title_short | Persistence of plasmid and tet(X4) in an Escherichia coli isolate coharboring blaNDM-5 and mcr-1 after acquiring an IncFII tet(X4)-positive plasmid |
| title_sort | persistence of plasmid and tet x4 in an escherichia coli isolate coharboring blandm 5 and mcr 1 after acquiring an incfii tet x4 positive plasmid |
| topic | blaNDM-5 mcr-1 tet(X4)-bearing plasmid plasmid stability tet(X4) stability |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1010387/full |
| work_keys_str_mv | AT xiaxiao persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT xiaxiao persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT ziyiliu persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT ziyiliu persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT xiaojunchen persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT xiaojunchen persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT kaipeng persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT kaipeng persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT ruichaoli persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT ruichaoli persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT ruichaoli persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT yuanliu persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT yuanliu persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT yuanliu persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT zhiqiangwang persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid AT zhiqiangwang persistenceofplasmidandtetx4inanescherichiacoliisolatecoharboringblandm5andmcr1afteracquiringanincfiitetx4positiveplasmid |