Benefits of a Recombination-Proficient Escherichia coli System for Adaptive Laboratory Evolution

Abstract

Adaptive laboratory evolution typically involves the propagation of organisms asexually to select for mutants with the desired phenotypes. However, asexual evolution is prone to competition among beneficial mutations (clonal interference) and the accumulation of hitchhiking and neutral mutations. The benefits of horizontal gene transfer toward overcoming these known disadvantages of asexual evolution were characterized in a strain of Escherichia coli engineered for superior sexual recombination (genderless). Specifically, we experimentally validated the capacity of the genderless strain to reduce the mutational load and recombine beneficial mutations. We also confirmed that inclusion of multiple origins of transfer influences both the frequency of genetic exchange throughout the chromosome and the linkage of donor DNA. We built a simple kinetic model to estimate recombination frequency as a function of transfer size and relative genotype enrichment in batch transfers; the model output correlated well with the experimental data. Our results provide strong support for the advantages of utilizing the genderless strain over its asexual counterpart during adaptive laboratory evolution for generating beneficial mutants with reduced mutational load. IMPORTANCEOver 80 years ago Fisher and Muller began a debate on the origins of sexual recombination. Although many aspects of sexual recombination have been examined at length, experimental evidence behind the behaviors of recombination in many systems and the means to harness it remain elusive. In this study, we sought to experimentally validate some advantages of recombination in typically asexual Escherichia coli and determine if a sexual strain of E. coli can become an effective tool for strain development.

Microbial Experimental Evolution – a proving ground for evolutionary theory and a tool for discovery

“…Experimental evolution of HGT in bacteria has been more difficult to study; however, recombination has been incorporated into E. coli experiments using conjugation systems . One of these studies confirmed results in S. cerevisiae that incorporating recombination into an experimental system will speed up adaptation .…”

No genome is an island: toward a 21st century agenda for evolution

“…The results in these more complex experimental environments are clear in showing the evolutionary benefits of mixed microbial populations. Accelerated adaptive evolution occurs when bacterial cultures are capable of intercellular DNA exchange In the development of novel yeast strains adapted to stressful fermentation conditions (high temperatures, high ethanol concentrations), interspecific hybrids are the products of selection for the most effective cultures …”

“…r Accelerated adaptive evolution occurs when bacterial cultures are capable of intercellular DNA exchange. 195,196 r In the development of novel yeast strains adapted to stressful fermentation conditions (high temperatures, high ethanol concentrations), interspecific hybrids are the products of selection for the most effective cultures. 197 The accumulating data on introgression and hybridization qqq in eukaryotic species of all kinds (yeasts, plants, animals) make it possible that the majority of adaptive innovations occur in periods of genome restructuring that follow interspecific crosses (see above).…”

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

“…More generally, studies that expose evolving populations to nutrient-limiting conditions, unusual carbon sources, or stressful environments (e.g. containing antibiotics) tend to show that sexually recombining populations can outperform asexual populations (Zeyl & Bell, 1997;Goddard et al, 2005;Cooper, 2007;Gray & Goddard, 2012;Winkler & Kao, 2012;Peabody et al, 2016). Removal of deleterious alleles may play an important role in such beneficial recombination (Zeyl & Bell, 1997;Cooper, 2007;Peabody et al, 2016).…”

“…containing antibiotics) tend to show that sexually recombining populations can outperform asexual populations (Zeyl & Bell, 1997;Goddard et al, 2005;Cooper, 2007;Gray & Goddard, 2012;Winkler & Kao, 2012;Peabody et al, 2016). Removal of deleterious alleles may play an important role in such beneficial recombination (Zeyl & Bell, 1997;Cooper, 2007;Peabody et al, 2016). Quantitatively and qualitatively different effects of recombination on adaptation in such studies may have various causes, including the kinds of adaptation considered, the number of loci underlying an adaptive trait and the fitness effects of individual mutations.…”