Transposable Elements Mediate Adaptive Debilitation of Flagella in Experimental Escherichia coli Populations.

Although insertion sequence (IS) elements are generally considered genomic parasites, they can mediate adaptive genetic changes in bacterial genomes. We discovered that among 12 laboratory-evolved Escherichia coli populations, three had experienced at least six different IS1-mediated deletions of flagellar genes. These deletions all involved the master flagellar regulator flhDC, and as such completely incapacitate motility. Two lines of evidence strongly suggest that these deletions were adaptive in our evolution experiment: (1) parallel evolution in three independent populations is highly unlikely just by chance, and (2) one of these deletion mutations swept to fixation within ~1000 generations, which is over two million times faster than expected if this deletion was instead selectively neutral and thus evolving by genetic drift. Because flagella are energetically expensive to synthesize and operate, we suspect that debilitating their construction conferred a fitness advantage in our well-stirred evolution experiment. These findings underscore the important role that IS elements can play in mediating adaptive loss-of-function mutations in bacteria.

Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli.

Insertion sequences (ISs) are transposable genetic elements in bacterial genomes. IS elements are common among bacteria but are generally rare within free-living species, probably because of the negative fitness effects they have on their hosts. Conversely, ISs frequently proliferate in intracellular symbionts and pathogens that recently transitioned from a free-living lifestyle. IS elements can profoundly influence the genomic evolution of their bacterial hosts, although it is unknown why they often expand in intracellular bacteria. We designed a laboratory evolution experiment with Escherichia coli K-12 to test the hypotheses that IS elements often expand in intracellular bacteria because of relaxed natural selection due to (1) their generally small effective population sizes (N (e)) and thus enhanced genetic drift, and (2) their nutrient rich environment, which makes many biosynthetic genes unnecessary and thus selectively neutral territory for IS insertion. We propagated 12 populations under four experimental conditions: large N (e) versus small N (e), and nutrient rich medium versus minimal medium. We found that relaxed selection over 4,000 generations was not sufficient to permit IS element expansion in any experimental population, thus leading us to hypothesize that IS expansion in intracellular symbionts may often be spurred by enhanced transposition rates, possibly due to environmental stress, coupled with relaxed natural selection.