KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide
Abstract Background Clinically important lineages in Klebsiella, especially those expressing multi-drug resistance (MDR), pose severe threats to public health worldwide. They arose from the co-evolution of the vertically inherited core genome and horizontal gene transfers by plasmids, which has not...
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2024-11-01
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| Series: | Genome Medicine |
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| Online Access: | https://doi.org/10.1186/s13073-024-01399-0 |
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| author | Heng Li Xiao Liu Shengkai Li Jie Rong Shichang Xie Yuan Gao Ling Zhong Quangui Jiang Guilai Jiang Yi Ren Wanping Sun Yuzhi Hong Zhemin Zhou |
| author_facet | Heng Li Xiao Liu Shengkai Li Jie Rong Shichang Xie Yuan Gao Ling Zhong Quangui Jiang Guilai Jiang Yi Ren Wanping Sun Yuzhi Hong Zhemin Zhou |
| author_sort | Heng Li |
| collection | DOAJ |
| description | Abstract Background Clinically important lineages in Klebsiella, especially those expressing multi-drug resistance (MDR), pose severe threats to public health worldwide. They arose from the co-evolution of the vertically inherited core genome and horizontal gene transfers by plasmids, which has not been systematically explored. Methods We designed KleTy, which consists of dedicated typing schemes for both the core genome and plasmids in Klebsiella. We compared the performance of KleTy with many state-of-the-art pipelines using both simulated and real data. Results Employing KleTy, we genotyped 33,272 Klebsiella genomes, categorizing them into 1773 distinct populations and predicting the presence of 87,410 plasmids from 837 clusters (PCs). Notably, Klebsiella is the center of the plasmid-exchange network within Enterobacteriaceae. Our results associated the international emergence of prevalent Klebsiella populations with only four carbapenem-resistance (CR) PCs, two hypervirulent PCs, and two hvCR-PCs encoding both carbapenemase and hypervirulence. Furthermore, we observed the ongoing international emergence of bla NDM, accompanied by the replacement of the previously dominant population, bla KPC-encoding HC1360_8 (CC258), during 2003–2018, with the emerging bla NDM-encoding HC1360_3 (CC147) thereafter. Additionally, expansions of hypervirulent carbapenem-resistant Klebsiella pneumoniae (hvCRKP) were evidenced in both populations, driven by plasmids of MDR-hypervirulence convergences. Conclusions The study illuminates how the global genetic landscape of Klebsiella has been shaped by the co-evolution of both the core genome and the plasmids, underscoring the importance of surveillance and control of the dissemination of plasmids for curtailing the emergence of hvCRKPs. |
| format | Article |
| id | doaj-art-d8c1c0dc72f242988aa5c514b200733c |
| institution | Kabale University |
| issn | 1756-994X |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Medicine |
| spelling | doaj-art-d8c1c0dc72f242988aa5c514b200733c2024-11-17T12:39:46ZengBMCGenome Medicine1756-994X2024-11-0116112010.1186/s13073-024-01399-0KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwideHeng Li0Xiao Liu1Shengkai Li2Jie Rong3Shichang Xie4Yuan Gao5Ling Zhong6Quangui Jiang7Guilai Jiang8Yi Ren9Wanping Sun10Yuzhi Hong11Zhemin Zhou12Key Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityIotabiome Biotechnology IncCollege of Pharmaceutical Sciences, Soochow UniversityMOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-Infective Medicine, Institute of Molecular Enzymology, School of Biology and Basic Medical Science, Suzhou Medical College, Soochow UniversityKey Laboratory of Alkene-Carbon Fibres-Based Technology & Application for Detection of Major Infectious Diseases, Jiangsu Province Engineering Research Center of Precision Diagnostics and Therapeutics Development, Cancer Institute, Suzhou Medical College, Soochow UniversityAbstract Background Clinically important lineages in Klebsiella, especially those expressing multi-drug resistance (MDR), pose severe threats to public health worldwide. They arose from the co-evolution of the vertically inherited core genome and horizontal gene transfers by plasmids, which has not been systematically explored. Methods We designed KleTy, which consists of dedicated typing schemes for both the core genome and plasmids in Klebsiella. We compared the performance of KleTy with many state-of-the-art pipelines using both simulated and real data. Results Employing KleTy, we genotyped 33,272 Klebsiella genomes, categorizing them into 1773 distinct populations and predicting the presence of 87,410 plasmids from 837 clusters (PCs). Notably, Klebsiella is the center of the plasmid-exchange network within Enterobacteriaceae. Our results associated the international emergence of prevalent Klebsiella populations with only four carbapenem-resistance (CR) PCs, two hypervirulent PCs, and two hvCR-PCs encoding both carbapenemase and hypervirulence. Furthermore, we observed the ongoing international emergence of bla NDM, accompanied by the replacement of the previously dominant population, bla KPC-encoding HC1360_8 (CC258), during 2003–2018, with the emerging bla NDM-encoding HC1360_3 (CC147) thereafter. Additionally, expansions of hypervirulent carbapenem-resistant Klebsiella pneumoniae (hvCRKP) were evidenced in both populations, driven by plasmids of MDR-hypervirulence convergences. Conclusions The study illuminates how the global genetic landscape of Klebsiella has been shaped by the co-evolution of both the core genome and the plasmids, underscoring the importance of surveillance and control of the dissemination of plasmids for curtailing the emergence of hvCRKPs.https://doi.org/10.1186/s13073-024-01399-0Distributed cgMLSTPlasmidKlebsiella pneumoniaeMulti-drug resistanceHypervirulence |
| spellingShingle | Heng Li Xiao Liu Shengkai Li Jie Rong Shichang Xie Yuan Gao Ling Zhong Quangui Jiang Guilai Jiang Yi Ren Wanping Sun Yuzhi Hong Zhemin Zhou KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide Genome Medicine Distributed cgMLST Plasmid Klebsiella pneumoniae Multi-drug resistance Hypervirulence |
| title | KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide |
| title_full | KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide |
| title_fullStr | KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide |
| title_full_unstemmed | KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide |
| title_short | KleTy: integrated typing scheme for core genome and plasmids reveals repeated emergence of multi-drug resistant epidemic lineages in Klebsiella worldwide |
| title_sort | klety integrated typing scheme for core genome and plasmids reveals repeated emergence of multi drug resistant epidemic lineages in klebsiella worldwide |
| topic | Distributed cgMLST Plasmid Klebsiella pneumoniae Multi-drug resistance Hypervirulence |
| url | https://doi.org/10.1186/s13073-024-01399-0 |
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