Evolutionary trajectories of secondary replicons in multipartite genomes

Abstract Most bacterial genomes have a single chromosome that may be supplemented by smaller, dispensable plasmids. However, approximately 10% of bacteria with completely sequenced genomes, mostly pathogens and plant symbionts, have more than one stable large replicon. Some secondary replicons are species-specific, carrying pathogenicity or symbiotic factors. Other replicons are common on at least the genus level, carry house-keeping genes, and may have a size of several million base pairs. We analyzed the abundance and sizes of large secondary replicons in different groups of bacteria and identified two patterns in the evolution of multipartite genomes. In nine genera of four families, Pseudoalteromonadaceae, Burkholderiaceae, Vibrionaceae , and Brucellaceae , we observed a positive correlation between the sizes of the chromosome and the secondary replicon with the slope in the range of 0.6–1.2. This indicates that in these genera the replicons evolve in a coordinated manner, with comparable rates of gene gain/loss, hence supporting classification of such secondary replicons as ‘chromids’. The second, more common pattern, features gene gains and losses mainly occurring in the primary replicon, yielding a stable size of the secondary replicon. Such secondary replicons are usually present in only a low fraction of the genus’ species. Hence, such replicons behave as ‘megaplasmids’. A mixed situation was observed in symbiotic genera from the Rhizobiaceae family where the large secondary replicons are of stable size, but present in all species. These results may provide a general framework for understanding the evolution of genome complexity in prokaryotes. Significance Large secondary replicons are observed in representatives of many taxonomic groups of bacteria. Traditionally, they are referred to as second chromosomes, chromids , or megaplasmids , with little consistency, in particular because their evolution remains understudied. Here we demonstrate that the sizes of secondary replicons follow two main evolutionary trends: replicons whose size scales linearly with the size of the main chromosome (the suggested term chromids ) typically contain numerous essential genes (rRNA, tRNA, ribosomal proteins), while large secondary replicons of stable size (termed megaplasmids ) contain fewer or none such genes.