Article

Phage–host population dynamics promotes prophage acquisition in bacteria with innate immunity

  • Nature Ecology & Evolutionvolume 2pages359366 (2018)
  • doi:10.1038/s41559-017-0424-z
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Abstract

Temperate bacteriophages integrate in bacterial genomes as prophages and represent an important source of genetic variation for bacterial evolution, frequently transmitting fitness-augmenting genes such as toxins responsible for virulence of major pathogens. However, only a fraction of bacteriophage infections are lysogenic and lead to prophage acquisition, whereas the majority are lytic and kill the infected bacteria. Unless able to discriminate lytic from lysogenic infections, mechanisms of immunity to bacteriophages are expected to act as a double-edged sword and increase the odds of survival at the cost of depriving bacteria of potentially beneficial prophages. We show that although restriction–modification systems as mechanisms of innate immunity prevent both lytic and lysogenic infections indiscriminately in individual bacteria, they increase the number of prophage-acquiring individuals at the population level. We find that this counterintuitive result is a consequence of phage–host population dynamics, in which restriction–modification systems delay infection onset until bacteria reach densities at which the probability of lysogeny increases. These results underscore the importance of population-level dynamics as a key factor modulating costs and benefits of immunity to temperate bacteriophages.

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Acknowledgements

This work was funded by an HFSP Young Investigators’ grant (C.C.G.) and a grant from the United States National Institutes of Health (GM 091875) (B.R.L.). M.P. is a recipient of a DOC Fellowship of the Austrian Academy of Science at the Institute of Science and Technology Austria. The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007–2013) under REA Grant Agreement No. 291734. We wish to thank A. Bagwatt, R. Blumenthal, I. Kobayashi, S. Makovets, S. Moineau, I. Mruk and M. Szczelkun for providing us with RM plasmids and phages. We thank S. Abedon, N. Balaban, D. Siekhaus, G. Tkacik and members of the C.C.G. laboratory for in-depth discussions and comments on the manuscript. We especially thank V. Krishna KV for assistance with the experiments.

Author information

Affiliations

  1. Institute of Science and Technology Austria, Am Campus 1, Klosterneuburg, Austria

    • Maroš Pleška
    • , Moritz Lang
    •  & Călin C. Guet
  2. Zurich University of Applied Sciences, Campus Grüental, Wädenswil, Switzerland

    • Dominik Refardt
  3. Department of Biology, Emory University, Atlanta, GA, USA

    • Bruce R. Levin

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Contributions

C.C.G., B.R.L. and M.P. designed the research, M.P. performed the experiments and analysed data, D.R. constructed the λ kan phage, M.L. and M.P. constructed and analysed the model, and C.C.G., B.R.L., M.L. and M.P. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Călin C. Guet.

Supplementary information

  1. Supplementary Information

    Supplementary Figs. 1–9; Supplementary Tables 1–3; Supplementary Methods; Supplementary References.

  2. Life Sciences Reporting Summary