A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes
IncL/M broad-host-range conjugative plasmids are involved in the global spread of <i>bla</i><sub>OXA-48</sub> and the emergence of <i>bla</i><sub>NDM-1</sub>. The aim of this study was to evaluate the transmission potential of plasmids encoding the eme...
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-11-01
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| Series: | Antibiotics |
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| Online Access: | https://www.mdpi.com/2079-6382/11/11/1641 |
| _version_ | 1827645145072271360 |
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| author | María Getino María López-Díaz Nicholas Ellaby John Clark Matthew J. Ellington Roberto M. La Ragione |
| author_facet | María Getino María López-Díaz Nicholas Ellaby John Clark Matthew J. Ellington Roberto M. La Ragione |
| author_sort | María Getino |
| collection | DOAJ |
| description | IncL/M broad-host-range conjugative plasmids are involved in the global spread of <i>bla</i><sub>OXA-48</sub> and the emergence of <i>bla</i><sub>NDM-1</sub>. The aim of this study was to evaluate the transmission potential of plasmids encoding the emergent NDM-1 carbapenemase compared to the pandemic OXA-48. The conjugation rate and fitness cost of IncM2 and IncL plasmids encoding these carbapenemase genes were tested using a variety of host bacteria. Genomic analysis of uropathogenic <i>Escherichia coli</i> SAP1756 revealed that <i>bla</i><sub>NDM-1</sub> was encoded on an IncM2 plasmid, which also harboured <i>bla</i><sub>TEM-1</sub>, <i>ble</i><sub>MBL</sub> and <i>sul1</i> and was highly similar to plasmids isolated from the same geographical area. Conjugation experiments demonstrated that NDM-1 and OXA-48-carrying plasmids transfer successfully between different Enterobacterales species, both in vitro and in vivo. Interestingly, <i>E. coli</i> isolates tested as recipients belonging to phylogroups A, B1, D and F were able to receive IncM2 plasmid pSAP1756, while phylogroups B2, C, E and G were not permissive to its acquisition. In general, the IncL OXA-48-carrying plasmids tested transferred at higher rates than IncM2 harbouring NDM-1 and imposed a lower burden to their host, possibly due to the inactivation of the <i>tir</i> fertility inhibition gene and reflecting their worldwide dissemination. IncM2 plasmids carrying <i>bla</i><sub>NDM-1</sub> are considered emergent threats that need continuous monitoring. In addition to sequencing efforts, phenotypic analysis of conjugation rates and fitness cost are effective methods for estimating the pandemic potential of antimicrobial resistance plasmids. |
| first_indexed | 2024-03-09T18:31:18Z |
| format | Article |
| id | doaj.art-7540a1d4b7d546d59e1a3d88995e7159 |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-09T18:31:18Z |
| publishDate | 2022-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-7540a1d4b7d546d59e1a3d88995e71592023-11-24T07:31:06ZengMDPI AGAntibiotics2079-63822022-11-011111164110.3390/antibiotics11111641A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase GenesMaría Getino0María López-Díaz1Nicholas Ellaby2John Clark3Matthew J. Ellington4Roberto M. La Ragione5Department of Comparative Biomedical Sciences, School of Veterinary Medicine, University of Surrey, Guildford GU2 7AL, UKUK Health Security Agency, Colindale, London NW9 5EQ, UKUK Health Security Agency, Colindale, London NW9 5EQ, UKDepartment of Microbiology, Epsom and St Helier University Hospitals NHS Trust, Carshalton SM5 1AA, UKUK Health Security Agency, Colindale, London NW9 5EQ, UKDepartment of Comparative Biomedical Sciences, School of Veterinary Medicine, University of Surrey, Guildford GU2 7AL, UKIncL/M broad-host-range conjugative plasmids are involved in the global spread of <i>bla</i><sub>OXA-48</sub> and the emergence of <i>bla</i><sub>NDM-1</sub>. The aim of this study was to evaluate the transmission potential of plasmids encoding the emergent NDM-1 carbapenemase compared to the pandemic OXA-48. The conjugation rate and fitness cost of IncM2 and IncL plasmids encoding these carbapenemase genes were tested using a variety of host bacteria. Genomic analysis of uropathogenic <i>Escherichia coli</i> SAP1756 revealed that <i>bla</i><sub>NDM-1</sub> was encoded on an IncM2 plasmid, which also harboured <i>bla</i><sub>TEM-1</sub>, <i>ble</i><sub>MBL</sub> and <i>sul1</i> and was highly similar to plasmids isolated from the same geographical area. Conjugation experiments demonstrated that NDM-1 and OXA-48-carrying plasmids transfer successfully between different Enterobacterales species, both in vitro and in vivo. Interestingly, <i>E. coli</i> isolates tested as recipients belonging to phylogroups A, B1, D and F were able to receive IncM2 plasmid pSAP1756, while phylogroups B2, C, E and G were not permissive to its acquisition. In general, the IncL OXA-48-carrying plasmids tested transferred at higher rates than IncM2 harbouring NDM-1 and imposed a lower burden to their host, possibly due to the inactivation of the <i>tir</i> fertility inhibition gene and reflecting their worldwide dissemination. IncM2 plasmids carrying <i>bla</i><sub>NDM-1</sub> are considered emergent threats that need continuous monitoring. In addition to sequencing efforts, phenotypic analysis of conjugation rates and fitness cost are effective methods for estimating the pandemic potential of antimicrobial resistance plasmids.https://www.mdpi.com/2079-6382/11/11/1641antimicrobial resistancecarbapenemaseEnterobacteralesplasmidconjugationIncL/M |
| spellingShingle | María Getino María López-Díaz Nicholas Ellaby John Clark Matthew J. Ellington Roberto M. La Ragione A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes Antibiotics antimicrobial resistance carbapenemase Enterobacterales plasmid conjugation IncL/M |
| title | A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes |
| title_full | A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes |
| title_fullStr | A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes |
| title_full_unstemmed | A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes |
| title_short | A Broad-Host-Range Plasmid Outbreak: Dynamics of IncL/M Plasmids Transferring Carbapenemase Genes |
| title_sort | broad host range plasmid outbreak dynamics of incl m plasmids transferring carbapenemase genes |
| topic | antimicrobial resistance carbapenemase Enterobacterales plasmid conjugation IncL/M |
| url | https://www.mdpi.com/2079-6382/11/11/1641 |
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