Bacteriophages limit the existence conditions for conjugative plasmids

Ellie Harrison, Jamie A. Wood, Calvin Dytham, Jonathan W. Pitchford, Julie Truman, Andrew J. Spiers, Steve Paterson, Michael A. Brockhurst

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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.
Original languageEnglish
Article numbere00586-15
Number of pages9
JournalmBio
Volume6
Issue number3
DOIs
Publication statusPublished - 2 Jun 2015

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Bacteriophages
Plasmids
Population Genetics
Bacterial Chromosomes
Bacteria
Mutation
Genetic Selection
Maintenance
Mortality
Population

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Harrison, E., Wood, J. A., Dytham, C., Pitchford, J. W., Truman, J., Spiers, A. J., ... Brockhurst, M. A. (2015). Bacteriophages limit the existence conditions for conjugative plasmids. mBio, 6(3), [e00586-15]. https://doi.org/10.1128/mBio.00586-15
Harrison, Ellie ; Wood, Jamie A. ; Dytham, Calvin ; Pitchford, Jonathan W. ; Truman, Julie ; Spiers, Andrew J. ; Paterson, Steve ; Brockhurst, Michael A. / Bacteriophages limit the existence conditions for conjugative plasmids. In: mBio. 2015 ; Vol. 6, No. 3.
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Harrison, E, Wood, JA, Dytham, C, Pitchford, JW, Truman, J, Spiers, AJ, Paterson, S & Brockhurst, MA 2015, 'Bacteriophages limit the existence conditions for conjugative plasmids', mBio, vol. 6, no. 3, e00586-15. https://doi.org/10.1128/mBio.00586-15

Bacteriophages limit the existence conditions for conjugative plasmids. / Harrison, Ellie; Wood, Jamie A.; Dytham, Calvin; Pitchford, Jonathan W.; Truman, Julie; Spiers, Andrew J.; Paterson, Steve; Brockhurst, Michael A.

In: mBio, Vol. 6, No. 3, e00586-15, 02.06.2015.

Research output: Contribution to journalArticle

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AU - Dytham, Calvin

AU - Pitchford, Jonathan W.

AU - Truman, Julie

AU - Spiers, Andrew J.

AU - Paterson, Steve

AU - Brockhurst, Michael A.

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AB - 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.

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Harrison E, Wood JA, Dytham C, Pitchford JW, Truman J, Spiers AJ et al. Bacteriophages limit the existence conditions for conjugative plasmids. mBio. 2015 Jun 2;6(3). e00586-15. https://doi.org/10.1128/mBio.00586-15