Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era.
Plasmids are diverse extrachromosomal elements significantly that contribute to interspecies dissemination of antimicrobial resistance (AMR) genes. However, within clinically important bacteria, plasmids can exhibit unexpected narrow host ranges, a phenomenon that has scarcely been examined. Here we...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2023-05-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010743 |
| _version_ | 1797812018181308416 |
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| author | Wearn-Xin Yee Muhammad Yasir A Keith Turner David J Baker Ana Cehovin Christoph M Tang |
| author_facet | Wearn-Xin Yee Muhammad Yasir A Keith Turner David J Baker Ana Cehovin Christoph M Tang |
| author_sort | Wearn-Xin Yee |
| collection | DOAJ |
| description | Plasmids are diverse extrachromosomal elements significantly that contribute to interspecies dissemination of antimicrobial resistance (AMR) genes. However, within clinically important bacteria, plasmids can exhibit unexpected narrow host ranges, a phenomenon that has scarcely been examined. Here we show that pConj is largely restricted to the human-specific pathogen, Neisseria gonorrhoeae. pConj can confer tetracycline resistance and is central to the dissemination of other AMR plasmids. We tracked pConj evolution from the pre-antibiotic era 80 years ago to the modern day and demonstrate that, aside from limited gene acquisition and loss events, pConj is remarkably conserved. Notably, pConj has remained prevalent in gonococcal populations despite cessation of tetracycline use, thereby demonstrating pConj adaptation to its host. Equally, pConj imposes no measurable fitness costs and is stably inherited by the gonococcus. Its maintenance depends on the co-operative activity of plasmid-encoded Toxin:Antitoxin (TA) and partitioning systems rather than host factors. An orphan VapD toxin encoded on pConj forms a split TA with antitoxins expressed from an ancestral co-resident plasmid or a horizontally-acquired chromosomal island, potentially explaining pConj's limited distribution. Finally, ciprofloxacin can induce loss of this highly stable plasmid, reflecting epidemiological evidence of transient reduction in pConj prevalence when fluoroquinolones were introduced to treat gonorrhoea. |
| first_indexed | 2024-03-13T07:32:19Z |
| format | Article |
| id | doaj.art-40f3ec4adcdd4292ab94a0c56d1e67ac |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-03-13T07:32:19Z |
| publishDate | 2023-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-40f3ec4adcdd4292ab94a0c56d1e67ac2023-06-04T05:31:51ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-05-01195e101074310.1371/journal.pgen.1010743Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era.Wearn-Xin YeeMuhammad YasirA Keith TurnerDavid J BakerAna CehovinChristoph M TangPlasmids are diverse extrachromosomal elements significantly that contribute to interspecies dissemination of antimicrobial resistance (AMR) genes. However, within clinically important bacteria, plasmids can exhibit unexpected narrow host ranges, a phenomenon that has scarcely been examined. Here we show that pConj is largely restricted to the human-specific pathogen, Neisseria gonorrhoeae. pConj can confer tetracycline resistance and is central to the dissemination of other AMR plasmids. We tracked pConj evolution from the pre-antibiotic era 80 years ago to the modern day and demonstrate that, aside from limited gene acquisition and loss events, pConj is remarkably conserved. Notably, pConj has remained prevalent in gonococcal populations despite cessation of tetracycline use, thereby demonstrating pConj adaptation to its host. Equally, pConj imposes no measurable fitness costs and is stably inherited by the gonococcus. Its maintenance depends on the co-operative activity of plasmid-encoded Toxin:Antitoxin (TA) and partitioning systems rather than host factors. An orphan VapD toxin encoded on pConj forms a split TA with antitoxins expressed from an ancestral co-resident plasmid or a horizontally-acquired chromosomal island, potentially explaining pConj's limited distribution. Finally, ciprofloxacin can induce loss of this highly stable plasmid, reflecting epidemiological evidence of transient reduction in pConj prevalence when fluoroquinolones were introduced to treat gonorrhoea.https://doi.org/10.1371/journal.pgen.1010743 |
| spellingShingle | Wearn-Xin Yee Muhammad Yasir A Keith Turner David J Baker Ana Cehovin Christoph M Tang Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. PLoS Genetics |
| title | Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. |
| title_full | Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. |
| title_fullStr | Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. |
| title_full_unstemmed | Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. |
| title_short | Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era. |
| title_sort | evolution persistence and host adaption of a gonococcal amr plasmid that emerged in the pre antibiotic era |
| url | https://doi.org/10.1371/journal.pgen.1010743 |
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