Chromosomal capture of beneficial genes drives plasmids toward ecological redundancy

Plasmids are a ubiquitous feature of bacterial genomes, but the forces driving genes and phenotypes to become associated with plasmids are poorly understood. To address this problem, we compared the fitness effects of chromosomal and plasmid genes in the plant symbiont Rhizobium leguminosarum. The relative abundance of beneficial genes on plasmids was very low compared to the chromosome across niches that reflect key steps in plant colonization. Two lines of evidence support the hypothesis that this pattern emerges because evolutionary processes drive beneficial genes to move from plasmids to the bacterial chromosome. First, weakly beneficial genes that increased fitness in a single niche were evenly distributed between plasmids and the chromosome, whereas the chromosome was enriched for strongly beneficial genes that increased fitness across multiple niches. Second, beneficial genes were more prevalent on recently acquired plasmids compared to ancient plasmids. Our findings support a model in which bacterial lineages initially acquire plasmids due to the beneficial genes that they carry, but the movement of beneficial genes to the chromosome gradually erodes the ecological value of plasmids. These findings reconcile existing models of plasmids and highlight the challenge of understanding how plasmids can persist over the long term.