Genomic analysis of a key innovation in an experimental Escherichia coli population

Abstract

Evolutionary novelties have been important in the history of life, but their origins are usually difficult to examine in detail. We previously described the evolution of a novel trait, aerobic citrate utilization (Cit+), in an experimental population of Escherichia coli. Here we analyze genome sequences to investigate the history and genetic basis of this trait. At least three distinct clades coexisted for more than 10,000 generations prior to its emergence. The Cit+ trait originated in one clade by a tandem duplication that captured an aerobically-expressed promoter for the expression of a previously silent citrate transporter. The clades varied in their propensity to evolve this novel trait, although genotypes able to do so existed in all three clades, implying that multiple potentiating mutations arose during the population’s history. Our findings illustrate the importance of promoter capture and altered gene regulation in mediating the exaptation events that often underlie evolutionary innovations.

Innovation: an emerging focus from cells to societies

“…the Dykhuizen-Hartl effect [94]), or are positively selected and increase in frequency until the novel trait is fully formed and spreads through the population [95 -97]. For example, Blount et al [95] experimentally demonstrated how multiple clades of Escherichia coli persisted for over 10 000 generations before a citrate metabolism trait arose in one lineage through the capture of a promoter exapting a previously silent duplication of the citrate transporter. Wallbank et al [97] showed that introgression between lineages of Heliconius butterflies can produce novel colour patterns based on the recombinatory shuffling of cis-regulatory modules.…”

Microbial Speciation

“…Hence, the model suggests that natural selection should be required to produce stable genotypic clusters, and that neutral cluster formation is extremely unlikely-a prediction that is borne out in longterm microbial experimental evolution studies. These studies have provided evidence that most fixed mutations tend to be adaptive, not neutral (Barrick et al 2009), and that formation of new genotypic clusters might involve adaptation to using novel resources (Blount et al 2012).…”

Repeated triggering of sporulation in Bacillus subtilis selects against a protein that affects the timing of cell division

“…Next-generation sequencing has revolutionized experimental evolution as a tool for studying the molecular basis of evolutionary adaptations on a genome scale (Barrick et al, 2009;Blount et al, 2012). Experimental evolution has successfully been used for studying, amongst others, cellular decision making.…”