Polyploid cyanobacterial genomes provide a reservoir of mutations, allowing rapid evolution of herbicide resistance.

Adaptive mechanisms in bacteria, which are widely assumed to be haploid or partially diploid, are thought to rely on the emergence of spontaneous mutations or lateral gene transfer from a reservoir of pre-existing variants within the surrounding environment. These variants then become fixed in the population upon exposure to selective pressures. Here, we show that multiple distinct wild-type (WT) substrains of the highly polyploid cyanobacterium Synechocystis sp. PCC 6803 can adapt rapidly to the potent herbicide methyl viologen (MV). Genome sequencing revealed that the mutations responsible for adaptation to MV were already present prior to selection in the genomes of the unadapted parental strains at low allelic frequencies. This indicates that chromosomal polyploidy in bacteria can provide cells with a reservoir of conditionally beneficial mutations that can become rapidly enriched and fixed upon selection. MV-resistant strains performed oxygenic photosynthesis less efficiently than WTs when MV was absent, suggesting trade-offs in cellular fitness associated with the evolution of MV resistance and a possible role for balancing selection in the maintenance of these alleles under ecologically relevant growth conditions. Resistance was associated with reduced intracellular accumulation of MV. Our results indicate that genome polyploidy plays a role in the rapid adaptation of some bacteria to stressful conditions, which may include xenobiotics, nutrient limitation, environmental stresses, and seasonal changes.