Mobile Compensatory Mutations Promote Plasmid Survival

ABSTRACT The global dissemination of plasmids encoding antibiotic resistance represents an urgent issue for human health and society. While the fitness costs for host cells associated with plasmid acquisition are expected to limit plasmid dissemination in the absence of positive selection of plasmid...

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Autores principales:	Martin Zwanzig, Ellie Harrison, Michael A. Brockhurst, James P. J. Hall, Thomas U. Berendonk, Uta Berger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	compensatory evolution chromosomal mutation plasmid mutation plasmid persistence fitness costs cost compensation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3a92a01fcabf4dfb8988c66de6ad9e89
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spelling	oai:doaj.org-article:3a92a01fcabf4dfb8988c66de6ad9e892021-12-02T19:47:34ZMobile Compensatory Mutations Promote Plasmid Survival10.1128/mSystems.00186-182379-5077https://doaj.org/article/3a92a01fcabf4dfb8988c66de6ad9e892019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00186-18https://doaj.org/toc/2379-5077ABSTRACT The global dissemination of plasmids encoding antibiotic resistance represents an urgent issue for human health and society. While the fitness costs for host cells associated with plasmid acquisition are expected to limit plasmid dissemination in the absence of positive selection of plasmid traits, compensatory evolution can reduce this burden. Experimental data suggest that compensatory mutations can be located on either the chromosome or the plasmid, and these are likely to have contrasting effects on plasmid dynamics. Whereas chromosomal mutations are inherited vertically through bacterial fission, plasmid mutations can be inherited both vertically and horizontally and potentially reduce the initial cost of the plasmid in new host cells. Here we show using mathematical models and simulations that the dynamics of plasmids depends critically on the genomic location of the compensatory mutation. We demonstrate that plasmid-located compensatory evolution is better at enhancing plasmid persistence, even when its effects are smaller than those provided by chromosomal compensation. Moreover, either type of compensatory evolution facilitates the survival of resistance plasmids at low drug concentrations. These insights contribute to an improved understanding of the conditions and mechanisms driving the spread and the evolution of antibiotic resistance plasmids. IMPORTANCE Understanding the evolutionary forces that maintain antibiotic resistance genes in a population, especially when antibiotics are not used, is an important problem for human health and society. The most common platform for the dissemination of antibiotic resistance genes is conjugative plasmids. Experimental studies showed that mutations located on the plasmid or the bacterial chromosome can reduce the costs plasmids impose on their hosts, resulting in antibiotic resistance plasmids being maintained even in the absence of antibiotics. While chromosomal mutations are only vertically inherited by the daughter cells, plasmid mutations are also provided to bacteria that acquire the plasmid through conjugation. Here we demonstrate how the mode of inheritance of a compensatory mutation crucially influences the ability of plasmids to spread and persist in a bacterial population.Martin ZwanzigEllie HarrisonMichael A. BrockhurstJames P. J. HallThomas U. BerendonkUta BergerAmerican Society for Microbiologyarticlecompensatory evolutionchromosomal mutationplasmid mutationplasmid persistencefitness costscost compensationMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	compensatory evolution chromosomal mutation plasmid mutation plasmid persistence fitness costs cost compensation Microbiology QR1-502
spellingShingle	compensatory evolution chromosomal mutation plasmid mutation plasmid persistence fitness costs cost compensation Microbiology QR1-502 Martin Zwanzig Ellie Harrison Michael A. Brockhurst James P. J. Hall Thomas U. Berendonk Uta Berger Mobile Compensatory Mutations Promote Plasmid Survival
description	ABSTRACT The global dissemination of plasmids encoding antibiotic resistance represents an urgent issue for human health and society. While the fitness costs for host cells associated with plasmid acquisition are expected to limit plasmid dissemination in the absence of positive selection of plasmid traits, compensatory evolution can reduce this burden. Experimental data suggest that compensatory mutations can be located on either the chromosome or the plasmid, and these are likely to have contrasting effects on plasmid dynamics. Whereas chromosomal mutations are inherited vertically through bacterial fission, plasmid mutations can be inherited both vertically and horizontally and potentially reduce the initial cost of the plasmid in new host cells. Here we show using mathematical models and simulations that the dynamics of plasmids depends critically on the genomic location of the compensatory mutation. We demonstrate that plasmid-located compensatory evolution is better at enhancing plasmid persistence, even when its effects are smaller than those provided by chromosomal compensation. Moreover, either type of compensatory evolution facilitates the survival of resistance plasmids at low drug concentrations. These insights contribute to an improved understanding of the conditions and mechanisms driving the spread and the evolution of antibiotic resistance plasmids. IMPORTANCE Understanding the evolutionary forces that maintain antibiotic resistance genes in a population, especially when antibiotics are not used, is an important problem for human health and society. The most common platform for the dissemination of antibiotic resistance genes is conjugative plasmids. Experimental studies showed that mutations located on the plasmid or the bacterial chromosome can reduce the costs plasmids impose on their hosts, resulting in antibiotic resistance plasmids being maintained even in the absence of antibiotics. While chromosomal mutations are only vertically inherited by the daughter cells, plasmid mutations are also provided to bacteria that acquire the plasmid through conjugation. Here we demonstrate how the mode of inheritance of a compensatory mutation crucially influences the ability of plasmids to spread and persist in a bacterial population.
format	article
author	Martin Zwanzig Ellie Harrison Michael A. Brockhurst James P. J. Hall Thomas U. Berendonk Uta Berger
author_facet	Martin Zwanzig Ellie Harrison Michael A. Brockhurst James P. J. Hall Thomas U. Berendonk Uta Berger
author_sort	Martin Zwanzig
title	Mobile Compensatory Mutations Promote Plasmid Survival
title_short	Mobile Compensatory Mutations Promote Plasmid Survival
title_full	Mobile Compensatory Mutations Promote Plasmid Survival
title_fullStr	Mobile Compensatory Mutations Promote Plasmid Survival
title_full_unstemmed	Mobile Compensatory Mutations Promote Plasmid Survival
title_sort	mobile compensatory mutations promote plasmid survival
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/3a92a01fcabf4dfb8988c66de6ad9e89
work_keys_str_mv	AT martinzwanzig mobilecompensatorymutationspromoteplasmidsurvival AT ellieharrison mobilecompensatorymutationspromoteplasmidsurvival AT michaelabrockhurst mobilecompensatorymutationspromoteplasmidsurvival AT jamespjhall mobilecompensatorymutationspromoteplasmidsurvival AT thomasuberendonk mobilecompensatorymutationspromoteplasmidsurvival AT utaberger mobilecompensatorymutationspromoteplasmidsurvival
_version_	1718375954226610176

Mobile Compensatory Mutations Promote Plasmid Survival

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