Evolution of gene order in prokaryotes is driven primarily by gene gain and loss

Abstract

Evolution of bacterial and archaeal genomes is highly dynamic including extensive gene gain via horizontal gene transfer and gene loss as well as different types of genome rearrangements, such as inversions and translocations, so that gene order is not highly conserved even among closely related organisms. We sought to quantify the contributions of different genome dynamics processes to the evolution of the gene order relying on the recently developed "jump" model of gene translocation. The jump model has been completely solved analytically and provides the exact distribution of syntenic gene block lengths (SBL) in compared genomes based on gene translocations alone. Comparing the SBL distribution predicted by the jump model with the distributions empirically observed for multiple groups of closely related bacterial and archaeal genomes, we obtained robust estimates of the genome rearrangement to gene flux (gain and loss) ratio. In most groups of bacteria and archaea, this ratio was found to be on the order of 0.1 indicating that the loss of synteny in the evolution of bacteria and archaea is driven primarily by gene gain and loss rather than by gene translocation. SignificanceEvolution of bacterial and archaeal genomes is a highly dynamic process that includes extensive gene gain via horizontal gene transfer and gene loss as well as different types of genome rearrangements, so that gene order is not highly conserved even among closely related organisms. We developed a theoretical framework to quantify the contributions of different genome dynamics processes to the evolution of the gene order and found that in most groups of bacteria and archaea, the genome rearrangement to gene flux (combined gain and loss) is on the order of 0.1. Thus, the loss of genomic synteny in the evolution of bacteria and archaea appears to be driven primarily by gene gain and loss rather than by gene translocation.