Bacteriophages Limit the Existence Conditions for Conjugative Plasmids

ABSTRACT Bacteriophages are a major cause of bacterial mortality and impose strong selection on natural bacterial populations, yet their effects on the dynamics of conjugative plasmids have rarely been tested. We combined experimental evolution, mathematical modeling, and individual-based simulation...

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Autores principales:	Ellie Harrison, A. Jamie Wood, Calvin Dytham, Jonathan W. Pitchford, Julie Truman, Andrew Spiers, Steve Paterson, Michael A. Brockhurst
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/36b40a246d3b4308a9cf1b9c97813f51
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spelling	oai:doaj.org-article:36b40a246d3b4308a9cf1b9c97813f512021-11-15T15:49:02ZBacteriophages Limit the Existence Conditions for Conjugative Plasmids10.1128/mBio.00586-152150-7511https://doaj.org/article/36b40a246d3b4308a9cf1b9c97813f512015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00586-15https://doaj.org/toc/2150-7511ABSTRACT Bacteriophages are a major cause of bacterial mortality and impose strong selection on natural bacterial populations, yet their effects on the dynamics of conjugative plasmids have rarely been tested. We combined experimental evolution, mathematical modeling, and individual-based simulations to explain how the ecological and population genetics effects of bacteriophages upon bacteria interact to determine the dynamics of conjugative plasmids and their persistence. The ecological effects of bacteriophages on bacteria are predicted to limit the existence conditions for conjugative plasmids, preventing persistence under weak selection for plasmid accessory traits. Experiments showed that phages drove faster extinction of plasmids in environments where the plasmid conferred no benefit, but they also revealed more complex effects of phages on plasmid dynamics under these conditions, specifically, the temporary maintenance of plasmids at fixation followed by rapid loss. We hypothesized that the population genetic effects of bacteriophages, specifically, selection for phage resistance mutations, may have caused this. Further mathematical modeling and individual-based simulations supported our hypothesis, showing that conjugative plasmids may hitchhike with phage resistance mutations in the bacterial chromosome. IMPORTANCE Conjugative plasmids are infectious loops of DNA capable of transmitting DNA between bacterial cells and between species. Because plasmids often carry extra genes that allow bacteria to live in otherwise-inhospitable environments, their dynamics are central to understanding bacterial adaptive evolution. The plasmid-bacterium interaction has typically been studied in isolation, but in natural bacterial communities, bacteriophages, viruses that infect bacteria, are ubiquitous. Using experiments, mathematical models, and computer simulations we show that bacteriophages drive plasmid dynamics through their ecological and evolutionary effects on bacteria and ultimately limit the conditions allowing plasmid existence. These results advance our understanding of bacterial adaptation and show that bacteriophages could be used to select against plasmids carrying undesirable traits, such as antibiotic resistance.Ellie HarrisonA. Jamie WoodCalvin DythamJonathan W. PitchfordJulie TrumanAndrew SpiersSteve PatersonMichael A. BrockhurstAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ellie Harrison A. Jamie Wood Calvin Dytham Jonathan W. Pitchford Julie Truman Andrew Spiers Steve Paterson Michael A. Brockhurst Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
description	ABSTRACT Bacteriophages are a major cause of bacterial mortality and impose strong selection on natural bacterial populations, yet their effects on the dynamics of conjugative plasmids have rarely been tested. We combined experimental evolution, mathematical modeling, and individual-based simulations to explain how the ecological and population genetics effects of bacteriophages upon bacteria interact to determine the dynamics of conjugative plasmids and their persistence. The ecological effects of bacteriophages on bacteria are predicted to limit the existence conditions for conjugative plasmids, preventing persistence under weak selection for plasmid accessory traits. Experiments showed that phages drove faster extinction of plasmids in environments where the plasmid conferred no benefit, but they also revealed more complex effects of phages on plasmid dynamics under these conditions, specifically, the temporary maintenance of plasmids at fixation followed by rapid loss. We hypothesized that the population genetic effects of bacteriophages, specifically, selection for phage resistance mutations, may have caused this. Further mathematical modeling and individual-based simulations supported our hypothesis, showing that conjugative plasmids may hitchhike with phage resistance mutations in the bacterial chromosome. IMPORTANCE Conjugative plasmids are infectious loops of DNA capable of transmitting DNA between bacterial cells and between species. Because plasmids often carry extra genes that allow bacteria to live in otherwise-inhospitable environments, their dynamics are central to understanding bacterial adaptive evolution. The plasmid-bacterium interaction has typically been studied in isolation, but in natural bacterial communities, bacteriophages, viruses that infect bacteria, are ubiquitous. Using experiments, mathematical models, and computer simulations we show that bacteriophages drive plasmid dynamics through their ecological and evolutionary effects on bacteria and ultimately limit the conditions allowing plasmid existence. These results advance our understanding of bacterial adaptation and show that bacteriophages could be used to select against plasmids carrying undesirable traits, such as antibiotic resistance.
format	article
author	Ellie Harrison A. Jamie Wood Calvin Dytham Jonathan W. Pitchford Julie Truman Andrew Spiers Steve Paterson Michael A. Brockhurst
author_facet	Ellie Harrison A. Jamie Wood Calvin Dytham Jonathan W. Pitchford Julie Truman Andrew Spiers Steve Paterson Michael A. Brockhurst
author_sort	Ellie Harrison
title	Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
title_short	Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
title_full	Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
title_fullStr	Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
title_full_unstemmed	Bacteriophages Limit the Existence Conditions for Conjugative Plasmids
title_sort	bacteriophages limit the existence conditions for conjugative plasmids
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/36b40a246d3b4308a9cf1b9c97813f51
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Bacteriophages Limit the Existence Conditions for Conjugative Plasmids

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