Selection and Genome Plasticity as the Key Factors in the Evolution of Bacteria

Abstract

In prokaryotes, the number of genes in different functional classes shows apparent universal scaling with the total number of genes that can be approximated by a power law, with a sublinear, near-linear, or superlinear scaling exponent. These dependences are gene class specific but hold across the entire diversity of bacteria and archaea. Several models have been proposed to explain these universal scaling laws, primarily based on the specifics of the respective biological functions. However, a population-genetic theory of universal scaling is lacking. We employ a simple mathematical model for prokaryotic genome evolution, which, together with the analysis of 34 clusters of closely related bacterial genomes, allows us to identify the underlying factors that govern the evolution of the genome content. Evolution of the gene content is dominated by two functional class-specific parameters: selection coefficient and genome plasticity. The selection coefficient quantifies the fitness cost associated with deletion of a gene in a given functional class or the advantage of successful incorporation of an additional gene. Genome plasticity reflects both the availability of the genes of a given class in the external gene pool that is accessible to the evolving population and the ability of microbes to accommodate these genes in the short term, that is, the class-specific horizontal gene transfer barrier. The selection coefficient determines the gene loss rate, whereas genome plasticity is the principal determinant of the gene gain rate.

Are Antisense Proteins in Prokaryotes Functional?

“…However, the evolutionary etiology of biological systems is not always fully accessible to us (Ardern, 2018) and sometimes the history of selection in a lineage or for a particular gene may be inaccessible or the accessible parts incomplete in important ways. The genomic influence of different kinds of selection on bacterial genomes, including selective sweeps, background selection, positive selection, and purifying selection, remains a point of contention (Takeuchi et al, 2015;Bendall et al, 2016;Gibson and Eyre-Walker, 2019;Sela et al, 2019). Perhaps the most difficult issue here is how to characterize function in young genes, which may be subject to evolutionary forces lying anywhere along a spectrum between positive selection and purifying selection.…”

Are Antisense Proteins in Prokaryotes Functional?

“…However, the evolutionary etiology of biological systems is not always fully accessible to us (Ardern, 2018), and sometimes the history of selection in a lineage or for a particular gene may be inaccessible or the accessible parts incomplete in important ways. The genomic influence of different kinds of selection on bacterial genomes, including selective sweeps, background selection, positive selection, and purifying selection, remains a point of contention (Bendall et al, 2016, Takeuchi et al, 2015, Gibson and Eyre-Walker, 2019, Sela et al, 2019. Perhaps the most difficult issue here is how to characterize function in young genes, which may be somewhere along a spectrum between positive selection and purifying selection.…”

Horizontal gene transfer barrier shapes the evolution of prokaryotic pangenomes

“…In the course of long term evolution of microbes, the HGT barrier is likely to be broken episodically as a result of major changes in environmental conditions when extensive HGT favors survival [13,29]. Different functional classes of microbial genes show substantial differences in evolutionary plasticity, or in other words, are differentially affected by the HGT barrier [20]. Thus, analysis of pangenome dynamics separately for each class can be expected to reveal the interplay between the key factors of genome evolution.…”

“…4 and Table S1). In terms of genome evolution, the fast or slow turnover rates reflect the different average selective effects associated with gene deletion: losing a slow-turnover gene is associated with greater fitness cost than losing a fast-turnover gene [20]. The fraction of fast evolving genes varies from as low as 7% up to 40%, apparently, reflecting substantial differences in the pangenome dynamics among prokaryotes (Fig.…”