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Transposable temperate phages promote the evolution of divergent social strategies in Pseudomonas aeruginosa populations


O'Brien, Siobhán; Kümmerli, Rolf; Paterson, Steve; Winstanley, Craig; Brockhurst, Michael A (2019). Transposable temperate phages promote the evolution of divergent social strategies in Pseudomonas aeruginosa populations. Proceedings of the Royal Society of London, Series B: Biological Sciences, 286(1912):20191794.

Abstract

Transposable temperate phages randomly insert into bacterial genomes, providing increased supply and altered spectra ofmutations available to selection, thus opening alternative evolutionary trajectories. Transposable phages accelerate bacterial adaptation to new environments, but their effect on adaptation to the social environment is unclear. Using experimental evolution of Pseudomonas aeruginosa in iron-limited and iron-rich environments, where the cost of producing cooperative iron-chelating siderophores is high and low, respectively, we show that transposable phages promote divergence into extreme siderophore production phenotypes. Iron-limited populations with transposable phages evolved siderophore overproducing clones alongside siderophore non-producing cheats. Low siderophore production was associated with parallel mutations in pvd genes, encoding pyoverdine biosynthesis, and pqs genes, encoding quinolone signalling, while high siderophore production was associated with parallel mutations in phenazine-associated gene clusters. Notably, some of these parallel mutations were caused by phage insertional inactivation. These data suggest that transposable phages, which are widespread in microbial immunities, can mediate the evolutionary divergence of social strategies.

Abstract

Transposable temperate phages randomly insert into bacterial genomes, providing increased supply and altered spectra ofmutations available to selection, thus opening alternative evolutionary trajectories. Transposable phages accelerate bacterial adaptation to new environments, but their effect on adaptation to the social environment is unclear. Using experimental evolution of Pseudomonas aeruginosa in iron-limited and iron-rich environments, where the cost of producing cooperative iron-chelating siderophores is high and low, respectively, we show that transposable phages promote divergence into extreme siderophore production phenotypes. Iron-limited populations with transposable phages evolved siderophore overproducing clones alongside siderophore non-producing cheats. Low siderophore production was associated with parallel mutations in pvd genes, encoding pyoverdine biosynthesis, and pqs genes, encoding quinolone signalling, while high siderophore production was associated with parallel mutations in phenazine-associated gene clusters. Notably, some of these parallel mutations were caused by phage insertional inactivation. These data suggest that transposable phages, which are widespread in microbial immunities, can mediate the evolutionary divergence of social strategies.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Department of Quantitative Biomedicine
Dewey Decimal Classification:580 Plants (Botany)
Scopus Subject Areas:Life Sciences > General Biochemistry, Genetics and Molecular Biology
Life Sciences > General Immunology and Microbiology
Physical Sciences > General Environmental Science
Life Sciences > General Agricultural and Biological Sciences
Uncontrolled Keywords:Biology, microbiology, siderophore, temperate phage, cooperation, Pseudomonas aeruginosa, experimental evolution, co-evolution
Language:English
Date:9 October 2019
Deposited On:20 Jan 2020 10:30
Last Modified:01 Jan 2021 19:26
Publisher:Royal Society Publishing
ISSN:0962-8452
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1098/rspb.2019.1794
PubMed ID:31594506
Project Information:
  • : FunderH2020
  • : Grant ID681295
  • : Project TitleBactInd - Bacterial cooperation at the individual cell level
  • : FunderSNSF
  • : Grant ID31003A_182499
  • : Project TitleAn evolutionary ecology approach to disarm bacterial pathogens, control infections, and understand polymicrobial interactions inside hosts

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