Evolutionary trajectories of secondary replicons in multipartite genomes

Most bacterial genomes have a single chromosome that may be supplemented by smaller, dispensable plasmids. However, to date, 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. Moreover, such secondary replicons are usually present in only a low fraction of the genus' species. Hence, such replicons behave as 'megaplasmids'. A mixed behavior was observed in symbiotic genera from the Rhizobiaceae family (Rhizobium, Agrobacterium, Azospirillum, and Ensifer) with large, essential secondary replicons of stable size. These results may provide a general framework for understanding the evolution of genome complexity in prokaryotes.