Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids
Providencia as an opportunistic pathogen can cause serious infection, and moreover the emergence of multi-drug-resistant Providencia strains poses a potentially life-threatening risk to public health. However, a comprehensive genomic study to reveal the population structure and dissemination of Prov...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2023-12-01
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| Series: | Emerging Microbes and Infections |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/22221751.2023.2275596 |
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| author | Peng Wang Cuidan Li Zhe Yin Xiaoyuan Jiang Xinyue Li Xiaofei Mu Nier Wu Fei Chen Dongsheng Zhou |
| author_facet | Peng Wang Cuidan Li Zhe Yin Xiaoyuan Jiang Xinyue Li Xiaofei Mu Nier Wu Fei Chen Dongsheng Zhou |
| author_sort | Peng Wang |
| collection | DOAJ |
| description | Providencia as an opportunistic pathogen can cause serious infection, and moreover the emergence of multi-drug-resistant Providencia strains poses a potentially life-threatening risk to public health. However, a comprehensive genomic study to reveal the population structure and dissemination of Providencia is still lacking. In this study, we conducted a genomic epidemiology analysis on the 580 global sequenced Providencia isolates, including 257 ones sequenced in this study (42 ones were fully sequenced). We established a genome sequence-based species classification scheme for Providencia, redefining the conventional 11 Providencia species into seven genocomplexes that were further divided into 18 genospecies, providing an extensively updated reference for Providencia species discrimination based on the largest Providencia genome dataset to date. We then dissected the profile of antimicrobial resistance genes and the prevalence of multi-drug-resistant Providencia strains among these genocomplexes/genospecies, disclosing the presence of diverse and abundant antimicrobial resistance genes and high resistance ratios against multiple classes of drugs in Providencia. We further dissected the genetic basis for the spread of blaNDM-1 in Providencia. blaNDM-1 genes were mainly carried by five incompatible (Inc) groups of plasmids: IncC, IncW, IncpPROV114-NR, IncpCHS4.1-3, and IncpPrY2001, and the last three were newly designated in this study. By tracking the spread of blaNDM-1-carrying plasmids, IncC, IncpPROV114-NR, IncpCHS4.1-3, and IncpPrY2001 plasmids were found to be highly involved in parallel horizontal transfer or vertical clonal expansion of blaNDM-1 among Providencia. Overall, our study provided a comprehensive genomic view of species differentiation, antimicrobial resistance prevalence, and plasmid-mediated blaNDM-1 dissemination in Providencia. |
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| id | doaj.art-464c15864ca349a7bde6b08efe6f7374 |
| institution | Directory Open Access Journal |
| issn | 2222-1751 |
| language | English |
| last_indexed | 2025-03-21T13:43:56Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
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| series | Emerging Microbes and Infections |
| spelling | doaj.art-464c15864ca349a7bde6b08efe6f73742024-06-26T10:39:28ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112210.1080/22221751.2023.2275596Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmidsPeng Wang0Cuidan Li1Zhe Yin2Xiaoyuan Jiang3Xinyue Li4Xiaofei Mu5Nier Wu6Fei Chen7Dongsheng Zhou8State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaProvidencia as an opportunistic pathogen can cause serious infection, and moreover the emergence of multi-drug-resistant Providencia strains poses a potentially life-threatening risk to public health. However, a comprehensive genomic study to reveal the population structure and dissemination of Providencia is still lacking. In this study, we conducted a genomic epidemiology analysis on the 580 global sequenced Providencia isolates, including 257 ones sequenced in this study (42 ones were fully sequenced). We established a genome sequence-based species classification scheme for Providencia, redefining the conventional 11 Providencia species into seven genocomplexes that were further divided into 18 genospecies, providing an extensively updated reference for Providencia species discrimination based on the largest Providencia genome dataset to date. We then dissected the profile of antimicrobial resistance genes and the prevalence of multi-drug-resistant Providencia strains among these genocomplexes/genospecies, disclosing the presence of diverse and abundant antimicrobial resistance genes and high resistance ratios against multiple classes of drugs in Providencia. We further dissected the genetic basis for the spread of blaNDM-1 in Providencia. blaNDM-1 genes were mainly carried by five incompatible (Inc) groups of plasmids: IncC, IncW, IncpPROV114-NR, IncpCHS4.1-3, and IncpPrY2001, and the last three were newly designated in this study. By tracking the spread of blaNDM-1-carrying plasmids, IncC, IncpPROV114-NR, IncpCHS4.1-3, and IncpPrY2001 plasmids were found to be highly involved in parallel horizontal transfer or vertical clonal expansion of blaNDM-1 among Providencia. Overall, our study provided a comprehensive genomic view of species differentiation, antimicrobial resistance prevalence, and plasmid-mediated blaNDM-1 dissemination in Providencia.https://www.tandfonline.com/doi/10.1080/22221751.2023.2275596Providenciagenome sequencingplasmidsantimicrobial resistanceblaNDM-1 |
| spellingShingle | Peng Wang Cuidan Li Zhe Yin Xiaoyuan Jiang Xinyue Li Xiaofei Mu Nier Wu Fei Chen Dongsheng Zhou Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids Emerging Microbes and Infections Providencia genome sequencing plasmids antimicrobial resistance blaNDM-1 |
| title | Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids |
| title_full | Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids |
| title_fullStr | Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids |
| title_full_unstemmed | Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids |
| title_short | Genomic epidemiology and heterogeneity of Providencia and their blaNDM-1-carrying plasmids |
| title_sort | genomic epidemiology and heterogeneity of providencia and their blandm 1 carrying plasmids |
| topic | Providencia genome sequencing plasmids antimicrobial resistance blaNDM-1 |
| url | https://www.tandfonline.com/doi/10.1080/22221751.2023.2275596 |
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