Chromosomal plasticity can drive rapid adaptation in bacteria

Understanding the molecular mechanisms underlying rapid adaptation to stress is a fundamental question in evolutionary biology. A common mechanism is copy number changes, which can affect single genes, larger genomic regions, or even entire chromosomes in the case of eukaryotes (aneuploidy). Bacterial species with genomes comprising more than one chromosome are common, yet the role of adaptive copy number changes affecting entire chromosomes is unknown. Here, by using a bacterium with two chromosomes (chrI and chrII) as model system and combining evolution experiments in the presence of severe nutrient stress with whole-genome sequencing, we show that chromosomal copy number changes can drive rapid adaptation. We detected increased copy number of the entire chrII in almost half of the sequenced clones, isolated from twelve independent populations. In most cases, copy number increases were driven by mutations in the replication protein of chrII. A higher chrII copy number is likely to be beneficial because chrII codes for the operon responsible for metabolizing D-gluconic acid, the only carbon source present in the medium. Our results revealed a novel mechanism for rapid adaptation in bacteria. Given the prevalence of bacteria with secondary chromosomes, and the enrichment of secondary chromosomes in genes associated with interaction with the environment, this may be an important mechanism for adapting to novel environments that has been overlooked.