The role of recombination in evolutionary adaptation of Escherichia coli to a novel nutrient

Abstract

The benefits and detriments of recombination for adaptive evolution have been studied both theoretically and experimentally, with conflicting predictions and observations. Most pertinent experiments examine recombination's effects in an unchanging environment and do not study its genomewide effects. Here, we evolved six replicate populations of either highly recombining R or lowly recombining R E. coli strains in a changing environment, by introducing the novel nutrients L-arabinose or indole into the environment. The experiment's ancestral strains are not viable on these nutrients, but 130 generations of adaptive evolution were sufficient to render them viable. Recombination conferred a more pronounced advantage to populations adapting to indole. To study the genomic changes associated with this advantage, we sequenced the genomes of 384 clones isolated from selected replicates at the end of the experiment. These genomes harbour complex changes that range from point mutations to large-scale DNA amplifications. Among several candidate adaptive mutations, those in the tryptophanase regulator tnaC stand out, because the tna operon in which it resides has a known role in indole metabolism. One of the highly recombining populations also shows a significant excess of large-scale segmental DNA amplifications that include the tna operon. This lineage also shows a unique and potentially adaptive combination of point mutations and DNA amplifications that may have originated independently from one another, to be joined later by recombination. Our data illustrate that the advantages of recombination for adaptive evolution strongly depend on the environment and that they can be associated with complex genomic changes.

Dynamics of genetic variation in Transcription Factors and its implications for the evolution of regulatory networks in Bacteria

“…For each study, we counted the number of non-synonymous mutations in TFs and TGs relative to the number of corresponding sites. 4 (29,34,35,39) out of 13 ALE studies (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39) had a significantly higher number of mutations in TFs than expected whereas none of the MA studies passed the significance test ( Fig. 5) (P One-sided Fisher's exact < 0.05 ).…”

“…Depending on the mode of action of the targeted drug(s) in a study, mutations may only be selected in a specific enzyme, in which case, an excess of TF's mutations would not be observed. This also holds for studies on auxotrophs (30). Often though, when a study focused on cross-resistance or on a drug with multiple mechanisms, selected mutations were more frequently among TFs (33,34,37) (Table S7, supplementary file 1).…”

“…Depending on the mode of action of the targeted drug(s) in a study, mutations may only be selected in a specific enzyme, in which case, an excess of TF's mutations would not be observed. This also holds for studies on auxotrophs (28). Often Fisher's exact test of the hypothesis that the frequency of mutations in TFs relative to TGs is greater than expected from the ratio of sites.…”

“…First, we identified 17 lab evolution projects with published (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43) information about the experimental design, 4 of which were MA studies (40)(41)(42)(43). For each study, we counted the number of non-synonymous mutations in TFs and TGs relative to the number of corresponding sites.…”

Sexual recombination and increased mutation rate expedite evolution of Escherichia coli in varied fitness landscapes

“…In work by McDonald et al 21 the ability of yeast to purge hitchhikers was demonstrated using sequence-level dynamics. Additionally in a recent work by Chu et al 29 using the genderless and an HFR control strains we had previously developed, a recombination event during in situ adaptive evolution was observed for the first time; however, the relative fitness impacts of the individual mutations and recombinants were not determined, thus the exact benefits of recombination were not fully assessed. In this work, we identified a specific case of a sexual recombination event that likely helped to maintain a weaker beneficial mutation (mutations in cyaA ) in the sexual population.…”