Synteny in Bacterial Genomes: Inference, Organization and Evolution

Abstract

Genes are not located randomly along genomes. Synteny, the conservation of their relative positions in genomes of different species, reflects fundamental constraints on natural evolution. We present approaches to infer pairs of co-localized genes from multiple genomes, describe their organization, and study their evolutionary history. In bacterial genomes, we thus identify synteny units, or "syntons", which are clusters of proximal genes that encompass and extend operons. The size distribution of these syntons divide them into large syntons, which correspond to fundamental macro-molecular complexes of bacteria, and smaller ones, which display a remarkable exponential distribution of sizes. This distribution is "universal" in two respects: it holds for vastly different genomes, and for functionally distinct genes. Similar statistical laws have been reported previously in studies of bacterial genomes, and generally attributed to purifying selection or neutral processes. Here, we perform a new analysis based on the concept of parsimony, and find that the prevailing evolutionary mechanism behind the formation of small syntons is a selective process of gene aggregation. Altogether, our results imply a common evolutionary process that selectively shapes the organization and diversity of bacterial genomes.