A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
ABSTRACT A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02528-21 |
| _version_ | 1818218505674162176 |
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| author | Han Wang Qi Xu Kaichao Chen Bill Kwan Wai Chan Lianwei Ye Xuemei Yang Miaomiao Xie Xiaobo Liu Hongyuhang Ni Edward Wai Chi Chan Sheng Chen |
| author_facet | Han Wang Qi Xu Kaichao Chen Bill Kwan Wai Chan Lianwei Ye Xuemei Yang Miaomiao Xie Xiaobo Liu Hongyuhang Ni Edward Wai Chi Chan Sheng Chen |
| author_sort | Han Wang |
| collection | DOAJ |
| description | ABSTRACT A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be common in E. coli from various sources. To understand the contribution of this plasmid to the virulence of E. coli, plasmid p1108-IncFIB in strain EC1108 was first cured to generate strain EC1108-PC. The virulence plasmid p15WZ-82_Vir in Klebsiella pneumoniae strain 15WZ-82 was then transmitted to EC1108-PC to produce the transconjugant, EC1108-PC-TC to assess the contribution of this virulence plasmid to the virulence level of E. coli. During the process of conjugation, p15WZ-82_Vir was found to be evolved into p15WZ-82_int, which underwent homologous recombination with a plasmid encoding a carbapenemase gene, blaNDM-1, p1108-NDM, in EC1108-PC. Comparison between the level of virulence in the EC1108, EC1108-PC-TC, and EC1108-PC through serum and macrophage resistance assay, as well as animal experiments, confirmed that plasmid p1108-IncFIB encoded a high level of virulence in E. coli, yet the fusion plasmid derived from p15WZ-82_Vir did not encode virulence but instead imposed a high fitness cost in the E. coli strain EC1108-PC-TC. These findings indicate that E. coli strains carrying the virulence plasmid p1108-IncFIB in multidrug-resistant (MDR) strains may also impose serious public health threats like that of hypervirulent Klebsiella pneumoniae strains harboring the p15WZ-82_Vir plasmid. IMPORTANCE Acquisition of pLVPK-like virulence plasmid by Klebsiella pneumoniae converts it to hypervirulent K. pneumoniae (HvKP), which has become one of the most important clinical bacterial pathogens. The potential of transmission of this virulence plasmid and its contribution to the virulence of other Enterobacteriaceae, such as E. coli, are not clear yet. In this study, we showed that pLVPK-like virulence plasmid exhibited fitness costs and did not contribute to the virulence in E. coli. However, we identified a novel virulence plasmid, p1108-IncFIB, that encodes similar siderophore genes as those of pLVPK from a foodborne E. coli strain and showed that p1108-IncFIB encoded a high level of virulence in E. coli. BLAST of E. coli genomes from GenBank showed that these siderophore genes were widespread in clinical E. coli strains. Further studies are warranted to understand the impact of this plasmid in the control of clinical infections caused by E. coli. |
| first_indexed | 2024-12-12T07:24:50Z |
| format | Article |
| id | doaj.art-7d26902390694c439e43432e5592987b |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-12T07:24:50Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj.art-7d26902390694c439e43432e5592987b2022-12-22T00:33:11ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.02528-21A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coliHan Wang0Qi Xu1Kaichao Chen2Bill Kwan Wai Chan3Lianwei Ye4Xuemei Yang5Miaomiao Xie6Xiaobo Liu7Hongyuhang Ni8Edward Wai Chi Chan9Sheng Chen10Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongNational Engineering Laboratory for Deep Process of Rice and By-Products, Hunan Key Laboratory of Grain-Oil Deep Process and Quality Control, Hunan Key Laboratory of Processed Food for Special Medical Purpose, College of Food Science and Engineering, Central South University of Forestry and Technology, Changsha, Hunan, ChinaDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongDepartment of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongABSTRACT A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be common in E. coli from various sources. To understand the contribution of this plasmid to the virulence of E. coli, plasmid p1108-IncFIB in strain EC1108 was first cured to generate strain EC1108-PC. The virulence plasmid p15WZ-82_Vir in Klebsiella pneumoniae strain 15WZ-82 was then transmitted to EC1108-PC to produce the transconjugant, EC1108-PC-TC to assess the contribution of this virulence plasmid to the virulence level of E. coli. During the process of conjugation, p15WZ-82_Vir was found to be evolved into p15WZ-82_int, which underwent homologous recombination with a plasmid encoding a carbapenemase gene, blaNDM-1, p1108-NDM, in EC1108-PC. Comparison between the level of virulence in the EC1108, EC1108-PC-TC, and EC1108-PC through serum and macrophage resistance assay, as well as animal experiments, confirmed that plasmid p1108-IncFIB encoded a high level of virulence in E. coli, yet the fusion plasmid derived from p15WZ-82_Vir did not encode virulence but instead imposed a high fitness cost in the E. coli strain EC1108-PC-TC. These findings indicate that E. coli strains carrying the virulence plasmid p1108-IncFIB in multidrug-resistant (MDR) strains may also impose serious public health threats like that of hypervirulent Klebsiella pneumoniae strains harboring the p15WZ-82_Vir plasmid. IMPORTANCE Acquisition of pLVPK-like virulence plasmid by Klebsiella pneumoniae converts it to hypervirulent K. pneumoniae (HvKP), which has become one of the most important clinical bacterial pathogens. The potential of transmission of this virulence plasmid and its contribution to the virulence of other Enterobacteriaceae, such as E. coli, are not clear yet. In this study, we showed that pLVPK-like virulence plasmid exhibited fitness costs and did not contribute to the virulence in E. coli. However, we identified a novel virulence plasmid, p1108-IncFIB, that encodes similar siderophore genes as those of pLVPK from a foodborne E. coli strain and showed that p1108-IncFIB encoded a high level of virulence in E. coli. BLAST of E. coli genomes from GenBank showed that these siderophore genes were widespread in clinical E. coli strains. Further studies are warranted to understand the impact of this plasmid in the control of clinical infections caused by E. coli.https://journals.asm.org/doi/10.1128/spectrum.02528-21conjugationvirulence plasmidavian pathogenic E. colihypervirulent K. pneumoniaetransmission |
| spellingShingle | Han Wang Qi Xu Kaichao Chen Bill Kwan Wai Chan Lianwei Ye Xuemei Yang Miaomiao Xie Xiaobo Liu Hongyuhang Ni Edward Wai Chi Chan Sheng Chen A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli Microbiology Spectrum conjugation virulence plasmid avian pathogenic E. coli hypervirulent K. pneumoniae transmission |
| title | A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli |
| title_full | A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli |
| title_fullStr | A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli |
| title_full_unstemmed | A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli |
| title_short | A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli |
| title_sort | siderophore encoding plasmid encodes high level virulence in escherichia coli |
| topic | conjugation virulence plasmid avian pathogenic E. coli hypervirulent K. pneumoniae transmission |
| url | https://journals.asm.org/doi/10.1128/spectrum.02528-21 |
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