Genome streamlining: effect of mutation rate and population size on genome size reduction

Abstract

Genome streamlining, i.e. genome size reduction, is observed in bacteria with very different life traits, including endosymbiotic bacteria and several marine bacteria, raising the question of its evolutionary origin. None of the hypotheses proposed in the literature is firmly established, mainly due to the many confounding factors related to the diverse habitats of species with streamlined genomes. Computational models may help overcome these difficulties and rigorously test hypotheses. In this work, we used Aevol, a platform designed to study the evolution of genome architecture, to test two main hypotheses: that an increase in population size (N) or mutation rate ({micro}) could cause genome reduction. In our experiments, both conditions lead to streamlining, but with very different resulting genome structures. Under increased population sizes, genomes loose a significant fraction of non-coding sequences, but maintain their coding size, resulting in densely packed genomes (akin to streamlined marine bacteria genomes). By contrast, under increased mutation rate, genomes loose both coding and non-coding sequences (akin to endosymbiotic bacteria genomes). Hence, both factors lead to an overall reduction in genome size, but the coding density of the genome appears to be determined by N x {micro}. Thus, a broad range of genome size and density can be achieved by different combinations of N and {micro}. Our results suggest that genome size and coding density are determined by the interplay between selection for phenotypic adaptation and selection for robustness. Significance statementMany bacterial species show reduced genomes. However, the diversity of these species and of their life traits makes it difficult to identify the mechanisms that led to this reduction. Indeed, no unifying hypothesis accounts for the whole diversity of genome size reduction. Here, we used simulations to systematically explore the effect of population size and mutation rate on genome size. We show that the interaction between these two factors tightly determine the size, but also the density of genomes, making it possible to account for the whole diversity of reduced genomes by acting on these two parameters only. Our results suggest a theoretical model in which genome reduction is driven by a robustness/fitness trade off.