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

Abstract
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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

Bram van Dijk

Theoretical Biology, Utrecht University, Utrecht, Netherlands

For correspondence
b.vandijk@uu.nl

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6330-6934
Paulien Hogeweg

Biology, Utrecht University, Utrecht, Netherlands

For correspondence
p.hogeweg@uu.nl

Competing interests
The authors declare that no competing interests exist.
Hilje M Doekes

Theoretical Biology, Utrecht University, Utrecht, Netherlands

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6360-5176
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 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.

Copyright

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.