Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health
ABSTRACT The emergence of plasmids coharboring hypervirulence (Hv) and multidrug resistance (MDR) genes has further accelerated the spread of MDR-Hv Klebsiella pneumoniae (MDR-HvKP) strains, having a severe impact on public health. Here, we report an MDR-Hv superplasmid coharboring hypervirulence an...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02634-22 |
| _version_ | 1811195032855642112 |
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| author | Xinmiao Jia Ying Zhu Peiyao Jia Xiaoyu Liu Wei Yu Xue Li Yingchun Xu Qiwen Yang |
| author_facet | Xinmiao Jia Ying Zhu Peiyao Jia Xiaoyu Liu Wei Yu Xue Li Yingchun Xu Qiwen Yang |
| author_sort | Xinmiao Jia |
| collection | DOAJ |
| description | ABSTRACT The emergence of plasmids coharboring hypervirulence (Hv) and multidrug resistance (MDR) genes has further accelerated the spread of MDR-Hv Klebsiella pneumoniae (MDR-HvKP) strains, having a severe impact on public health. Here, we report an MDR-Hv superplasmid coharboring hypervirulence and MDR genes and the detailed characterization of its genetic and phenotypic features. This plasmid was identified in an ST11 (sequence type 11)-K64 carbapenem-resistant hypervirulent K. pneumoniae (CR-HvKP) strain, SZS128, which was responsible for a bloodstream infection in a 21-year-old female. Susceptibility testing showed that SZS128 was resistant to amikacin, levofloxacin, and almost all of the β-lactams examined. SZS128 showed high virulence in a Galleria mellonella survival assay and a mouse intraperitoneal infection model. Genomic analysis showed that SZS128 not only possessed a KPC plasmid (pSZS128-KPC) but also carried a superplasmid (pSZS128-Hv-MDR) coharboring hypervirulence and MDR genes and possessing complete conjugative regions. Conjugation and transformation assays confirmed the potential for horizontal transfer and the high stability (retention rate of >95%) of the pSZS128-Hv-MDR superplasmid. Furthermore, growth curve assessment confirmed that there was no increase in the fitness cost in the presence of pSZS128-Hv-MDR. Therefore, we define a superplasmid as a plasmid fulfilling all the following criteria: (i) a single plasmid that coharbors hypervirulence and MDR genes, (ii) a plasmid that harbors complete conjugative elements that guarantee self-transmissibility, (iii) a plasmid that is stable and conserved, and (iv) a plasmid with no fitness cost to the host strain. The emergence of this kind of superplasmid could represent a serious threat to public health, and urgent control measures must be implemented. IMPORTANCE This self-transmissible superplasmid, which simultaneously carries hypervirulence and MDR genes, greatly enhances the challenges to clinical prevention and control and anti-infection treatment. Thus, active surveillance of this type of superplasmid is needed to prevent these efficient resistance/virulence plasmids from disseminating in hospital settings. Our findings provide a reference for defining the term “superplasmid” and emphasize the importance of raising public awareness of the rapid dissemination of this self-transmissible superplasmid and the consistent emergence of MDR-HvKP strains. |
| first_indexed | 2024-04-12T00:36:57Z |
| format | Article |
| id | doaj.art-fa26a0f3eee3401cae0947c06f3f9bf7 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T00:36:57Z |
| publishDate | 2022-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-fa26a0f3eee3401cae0947c06f3f9bf72022-12-22T03:55:08ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-12-0110610.1128/spectrum.02634-22Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public HealthXinmiao Jia0Ying Zhu1Peiyao Jia2Xiaoyu Liu3Wei Yu4Xue Li5Yingchun Xu6Qiwen Yang7Department of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaDepartment of Clinical Laboratory, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, ChinaABSTRACT The emergence of plasmids coharboring hypervirulence (Hv) and multidrug resistance (MDR) genes has further accelerated the spread of MDR-Hv Klebsiella pneumoniae (MDR-HvKP) strains, having a severe impact on public health. Here, we report an MDR-Hv superplasmid coharboring hypervirulence and MDR genes and the detailed characterization of its genetic and phenotypic features. This plasmid was identified in an ST11 (sequence type 11)-K64 carbapenem-resistant hypervirulent K. pneumoniae (CR-HvKP) strain, SZS128, which was responsible for a bloodstream infection in a 21-year-old female. Susceptibility testing showed that SZS128 was resistant to amikacin, levofloxacin, and almost all of the β-lactams examined. SZS128 showed high virulence in a Galleria mellonella survival assay and a mouse intraperitoneal infection model. Genomic analysis showed that SZS128 not only possessed a KPC plasmid (pSZS128-KPC) but also carried a superplasmid (pSZS128-Hv-MDR) coharboring hypervirulence and MDR genes and possessing complete conjugative regions. Conjugation and transformation assays confirmed the potential for horizontal transfer and the high stability (retention rate of >95%) of the pSZS128-Hv-MDR superplasmid. Furthermore, growth curve assessment confirmed that there was no increase in the fitness cost in the presence of pSZS128-Hv-MDR. Therefore, we define a superplasmid as a plasmid fulfilling all the following criteria: (i) a single plasmid that coharbors hypervirulence and MDR genes, (ii) a plasmid that harbors complete conjugative elements that guarantee self-transmissibility, (iii) a plasmid that is stable and conserved, and (iv) a plasmid with no fitness cost to the host strain. The emergence of this kind of superplasmid could represent a serious threat to public health, and urgent control measures must be implemented. IMPORTANCE This self-transmissible superplasmid, which simultaneously carries hypervirulence and MDR genes, greatly enhances the challenges to clinical prevention and control and anti-infection treatment. Thus, active surveillance of this type of superplasmid is needed to prevent these efficient resistance/virulence plasmids from disseminating in hospital settings. Our findings provide a reference for defining the term “superplasmid” and emphasize the importance of raising public awareness of the rapid dissemination of this self-transmissible superplasmid and the consistent emergence of MDR-HvKP strains.https://journals.asm.org/doi/10.1128/spectrum.02634-22carbapenemasemultidrug resistancehypervirulenceKlebsiella pneumoniaesuperplasmid |
| spellingShingle | Xinmiao Jia Ying Zhu Peiyao Jia Xiaoyu Liu Wei Yu Xue Li Yingchun Xu Qiwen Yang Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health Microbiology Spectrum carbapenemase multidrug resistance hypervirulence Klebsiella pneumoniae superplasmid |
| title | Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health |
| title_full | Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health |
| title_fullStr | Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health |
| title_full_unstemmed | Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health |
| title_short | Emergence of a Superplasmid Coharboring Hypervirulence and Multidrug Resistance Genes in Klebsiella pneumoniae Poses New Challenges to Public Health |
| title_sort | emergence of a superplasmid coharboring hypervirulence and multidrug resistance genes in klebsiella pneumoniae poses new challenges to public health |
| topic | carbapenemase multidrug resistance hypervirulence Klebsiella pneumoniae superplasmid |
| url | https://journals.asm.org/doi/10.1128/spectrum.02634-22 |
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