Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing.

BACKGROUND: Recombination is widespread across the tree of life, because it helps purge deleterious mutations and creates novel adaptive traits. In prokaryotes, it often takes the form of horizontal gene transfer from a donor to a recipient bacterium. While such transfer is widespread in natural communities, its immediate fitness benefits are usually unknown. We asked whether any such benefits depend on the environment, and on the identity of donor and recipient strains. To this end, we adapted Escherichia coli to two novel carbon sources over several hundred generations of laboratory evolution, exposing evolving populations to various DNA donors.

RESULTS: At the end of these experiments, we measured fitness and sequenced the genomes of 65 clones from 34 replicate populations to study the genetic changes associated with adaptive evolution. Furthermore, we identified candidate de novo beneficial mutations. During adaptive evolution on the first carbon source, 4-Hydroxyphenylacetic acid (HPA), recombining populations adapted better, which was likely mediated by acquiring the hpa operon from the donor. In contrast, recombining populations did not adapt better to the second carbon source, butyric acid, even though they suffered fewer extinctions than non-recombining populations. The amount of DNA transferred, but not its benefit, strongly depended on the donor-recipient strain combination.

CONCLUSIONS: To our knowledge, our study is the first to investigate the genomic consequences of prokaryotic recombination and horizontal gene transfer during laboratory evolution. It shows that the benefits of recombination strongly depend on the environment and the foreign DNA donor.