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

Abstract

BackgroundRecombination 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.ResultsAt 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.ConclusionsTo 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1164-7) contains supplementary material, which is available to authorized users.

Horizontal ‘gene drives’ harness indigenous bacteria for bioremediation

“…Our results also suggest native soil and marine microbial communities will continue to carry synthetic vectors with useful catabolic genes, likely until the metabolic cost of replicating the vector no longer presents an advantage. This agrees with previous studies which show that HGT transfer events that alter organism metabolism can increase organism fitness by allowing them to colonize new ecological niches 57,60,61 . It also suggests that this approach to engineering polluted ecosystems is self-limiting: selective pressure from the existing ecosystem could remove introduced genes from local microbial populations when no longer needed.…”

The emergence of adaptive laboratory evolution as an efficient tool for biological discovery and industrial biotechnology

“…Bacterial asexual reproduction leads to clonal interference, preventing many beneficial mutations from reaching fixation within the evolving populations. Chu et al investigated induced horizontal gene transfer as a method to speed adaptation and circumvent clonal interference, and found that genetic exchange between distinct cocultured E. coli strains could significantly aid in adaptation to growth on novel carbon sources, contingent on the specifics of donor vs. host strain similarity and evolutionary environment (Chu et al, 2018). Contrasting with horizontal gene transfer, another technique to increase the accessibility of adaptive mutations is simply to increase the mutation rate, which can be induced with chemical mutagens (Lee et al, 2011) or naturally result from a DNA repair gene deactivation (LaCroix et al, 2014;Lenski et al, 2015); in all cases, mutation rate positively correlated with the speed of adaptation and magnitude of fitness gains.…”

Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

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