Evolution of the Plant-Associated Pantoea was Accompanied by Plasmid Domestication Events

Plasmids are important drivers of evolutionary transformations and ecological adaptation in prokaryotes. Plasmids supplying the host with beneficial functions may become domesticated and gain a stable inheritance within the host lineage. Domesticated plasmids may comprise core genes that are present in all taxon members. The origin of plasmid core genes remains poorly understood and alternative scenarios entailing gene translocation or genetic redundancy are debated. Studying plasmid evolution in the plant-associated Pantoea, we show that the large Pantoea plasmids (LPP-1 and LPP-2) are domesticated. We infer that the LPP-1 was acquired in the ancestor of plant-associated Pantoea species. The LPP-2 acquisition is traced to the ancestor of plant growth-promoting species. We show that both plasmids are vertically inherited and the LPP-1 replication is furthermore coordinated with chromosome replication. Both plasmids harbor core gene families at the genus (LPP-1) or species (LPP-2) level. Using phylogenomics we infer a deep divergence between plasmid and chromosomal core genes, indicating rare gene translocation between the replicons. Our results suggest that the LPP-1 and LPP-2 acquisition introduced genetic redundancy with chromosomal genes, that was followed by successive waves of differential gene loss. The domestication of both plasmids likely contributed to species divergence in Pantoea.