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.