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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...

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Autores principales: Yee, Wearn-Xin, Yasir, Muhammad, Turner, A. Keith, Baker, David J., Cehovin, Ana, Tang, Christoph M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212123/
https://www.ncbi.nlm.nih.gov/pubmed/37186602
http://dx.doi.org/10.1371/journal.pgen.1010743
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author Yee, Wearn-Xin
Yasir, Muhammad
Turner, A. Keith
Baker, David J.
Cehovin, Ana
Tang, Christoph M.
author_facet Yee, Wearn-Xin
Yasir, Muhammad
Turner, A. Keith
Baker, David J.
Cehovin, Ana
Tang, Christoph M.
author_sort Yee, Wearn-Xin
collection PubMed
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.
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spelling pubmed-102121232023-05-26 Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era Yee, Wearn-Xin Yasir, Muhammad Turner, A. Keith Baker, David J. Cehovin, Ana Tang, Christoph M. PLoS Genet Research Article 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. Public Library of Science 2023-05-15 /pmc/articles/PMC10212123/ /pubmed/37186602 http://dx.doi.org/10.1371/journal.pgen.1010743 Text en © 2023 Yee et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yee, Wearn-Xin
Yasir, Muhammad
Turner, A. Keith
Baker, David J.
Cehovin, Ana
Tang, Christoph M.
Evolution, persistence, and host adaption of a gonococcal AMR plasmid that emerged in the pre-antibiotic era
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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212123/
https://www.ncbi.nlm.nih.gov/pubmed/37186602
http://dx.doi.org/10.1371/journal.pgen.1010743
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