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

Hilje M Doekes,Paulien Hogeweg,Bram Van Dijk,Nobuto Takeuchi

doi:10.7554/elife.56801

Hilje M Doekes, Paulien Hogeweg + Show 2 more

Open Access

https://doi.org/10.7554/elife.56801

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Journal: eLife	Publication Date: May 21, 2020
Citations: 34	License type: CC BY 4.0

Affiliation: Utrecht University, University of Auckland

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 bacterial 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 foreign DNA is evolutionarily maintained by the hosts, explaining the coexistence of bacteria and SGEs.

Highlights

Horizontal Gene Transfer (HGT), the transmission of genetic material between unrelated individuals, is a major factor driving prokaryotic evolution (Ochman et al, 2000; Doolittle and Zhaxybayeva, 2009; Vogan and Higgs, 2011)
Non-carriers can recover genes by interacting with carriers through HGT. We study these dynamics with different models, first using simple ordinary differential equations (ODEs, Figure 1A,B) and later an individual-based model (IBM) that takes spatial population structuring into account (Figure 1C)
We have studied the balance between the advantages and disadvantages of HGT by modelling a simple bacterial population undergoing the uptake of genes from a shared DNA pool

Summary

Introduction

Horizontal Gene Transfer (HGT), the transmission of genetic material between unrelated individuals, is a major factor driving prokaryotic evolution (Ochman et al, 2000; Doolittle and Zhaxybayeva, 2009; Vogan and Higgs, 2011). Recent estimates of the rate of HGT in closely related bacteria are staggeringly high (Iranzo et al, 2019; Sakoparnig, 2019), with HGT possibly even outpacing gradual sequence evolution (Hao and Golding, 2006; Puigboet al., 2014; Vos et al, 2015). Combining this with the fact that prokaryotes adapt mostly through rapid gene loss (Kuo and Ochman, 2009; Morris et al, 2012), bacterial adaptation appears to be mainly driven by changes in gene content (Snel et al, 2002; Treangen and Rocha, 2011; Nowell et al, 2014). Genes appear to be rapidly lost from any individual lineage, but are retained in a much larger gene pool through HGT

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