Genome plasticity, a key factor of evolution in prokaryotes

Abstract

In prokaryotic genomes, the number of genes that belong to distinct functional classes shows apparent universal scaling with the total number of genes [1–5] (Fig. 1). This scaling can be approximated with a power law, where the scaling power can be sublinear, near-linear or super-linear. Scaling laws are robust under various statistical tests [4], across different databases and for different gene classifications [1–5]. Several models aimed at explaining the observed scaling laws have been proposed, primarily, based on the specifics of the respective biological functions [1, 5–8]. However, a coherent theory to explain the emergence of scaling within the framework of population genetics is lacking. We employ a simple mathematical model for prokaryotic genome evolution [9] which, together with the analysis of 34 clusters of closely related microbial genomes [10], allows us to identify the underlying forces that dictate genome content evolution. In addition to the scaling of the number of genes in different functional classes, we explore gene contents divergence to characterize the evolutionary processes acting upon genomes [11]. We find that evolution of the gene content is dominated by two factors that are specific to a functional class, namely, selection landscape and genome plasticity. Selection landscape quantifies the fitness cost that is associated with deletion of a gene in a given functional class or the advantage of successful incorporation of an additional gene. Genome plasticity, that can be considered a measure of evolvability, reflects both the availability of the genes of a given functional class in the external gene pool that is accessible to the evolving microbial population, and the ability of microbial genomes to accommodate these genes. The selection landscape determines the gene loss rate, and genome plasticity is the principal determinant of the gene gain rate.