Slightly beneficial genes are retained by bacteria evolving DNA uptake despite selfish elements

  1. Bram van van Dijk  Is a corresponding author
  2. Paulien Hogeweg  Is a corresponding author
  3. Hilje M Doekes
  4. Nobuto Takeuchi
  1. Utrecht University, Netherlands
  2. University of Auckland, New Zealand

Abstract

Horizontal gene transfer (HGT) and gene loss result in rapid changes in the gene content of bacteria. While HGT aids bacteria to adapt to new environments, it also carries risks such as selfish genetic elements (SGEs). Here, we use modelling to study how HGT of slightly beneficial genes impacts growth rates of bacterial populations, and if bacteria collectives can evolve to take up DNA despite selfish elements. We find four classes of slightly beneficial genes: indispensable, enrichable, rescuable, and unrescuable genes. Rescuable genes — genes with small fitness benefits that are lost from the population without HGT — can be collectively retained by a community that engages in costly HGT. While this `gene-sharing' cannot evolve in well-mixed cultures, it does evolve in a spatial population like a biofilm. Despite enabling infection by harmful SGEs, the uptake of DNA is evolutionarily maintained by the hosts, explaining the coexistence of bacteria and SGEs.

Data availability

All data are either mathematical or computationally generated, and therefore easily reproduced. All scripts and programs to so do are publically available on GitHub (https://github.com/bramvandijk88/HGT_Genes_And_SGEs).For Figure 2 and 3 we used the analytical model. To (numerically) reproduce our results, use the Rscripts provided in the repository. For Figure 4, 5 and 6 we used the individual-based model. This was implemented in C, and can be run with simple command-line options (readme file found in the zip).

Article and author information

Author details

  1. Bram van van Dijk

    Theoretical Biology, Utrecht University, Utrecht, Netherlands
    For correspondence
    b.vandijk@uu.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6330-6934
  2. Paulien Hogeweg

    Biology, Utrecht University, Utrecht, Netherlands
    For correspondence
    p.hogeweg@uu.nl
    Competing interests
    The authors declare that no competing interests exist.
  3. Hilje M Doekes

    Theoretical Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6360-5176
  4. Nobuto Takeuchi

    School of Biological Sciences, University of Auckland, Auckland, New Zealand
    Competing interests
    The authors declare that no competing interests exist.

Funding

Seventh Framework Programme (ICT-610427)

  • Bram van van Dijk

Seventh Framework Programme (ICT-610427)

  • Paulien Hogeweg

Human Frontier Science Program (RGY0072/2015)

  • Hilje M Doekes

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sara Mitri, University of Lausanne, Switzerland

Publication history

  1. Received: March 10, 2020
  2. Accepted: May 15, 2020
  3. Accepted Manuscript published: May 20, 2020 (version 1)
  4. Accepted Manuscript updated: May 21, 2020 (version 2)
  5. Version of Record published: June 25, 2020 (version 3)

Copyright

© 2020, van Dijk et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Bram van van Dijk
  2. Paulien Hogeweg
  3. Hilje M Doekes
  4. Nobuto Takeuchi
(2020)
Slightly beneficial genes are retained by bacteria evolving DNA uptake despite selfish elements
eLife 9:e56801.
https://doi.org/10.7554/eLife.56801

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