Evolutionary Remodeling of Bacterial Motility Checkpoint Control

Abstract

SummaryRegulatory networks play a central role in the relationship between genotype and phenotype in all organisms. However, the mechanisms that underpin the evolutionary plasticity of these networks remain poorly understood. Here, we used experimental selection for enhanced bacterial motility in a porous environment to explore the adaptability of one of the most complex networks known in bacteria. We found that the resulting phenotypic changes are mediated by adaptive mutations in several functionally different proteins, including multiple components of the flagellar motor. Nevertheless, this evolutionary adaptation could be explained by a single mechanism, namely remodeling of the checkpoint regulating flagellar gene expression. Supported by computer simulations, our findings suggest that the specific “bow-tie” topology of the checkpoint facilitates evolutionary tuning of the cost-benefit trade-off between motility and growth. We propose that bow-tie regulatory motifs, which are widespread in cellular networks, play a general role in evolutionary adaptation.

Evolution at the Edge of Expanding Populations

“…Additional field examples of invasive populations, where margin individuals acquired greater dispersal and slower growth, include other plants (Ganeshaiah and Shaanker 1991;Huang et al 2015;Williams et al 2016), fish (Agostinho et al 2015), crickets (Simmons and Thomas 2004), butterflies (Hughes et al 2003), and fungi (Garbelotto et al 2015). Laboratory experiments with populations expanding towards a virgin territory with freshwater ciliates (Fronhofer and Altermatt 2015), beetles (Ochocki and Miller 2017;Weiss-Lehman et al 2017), plants (Williams et al 2016), and bacteria (Fraebel et al 2017;Ni et al 2017) led to similar results: population expansion can favor faster dispersal at the expense of slower growth.…”

Growth-rate dependent resource investment in bacterial motile behavior quantitatively follows potential benefit of chemotaxis

“…Relative Fitness Cost of Motility Depends on Carbon Source. In order to directly evaluate the costs and benefits of motility as a function of the N-value, we used pairwise growth competition between strains to assess their relative reproductive fitness under particular conditions (11,17). To monitor the ratio of 2 strains in cocultures using flow cytometry, we respectively labeled them with either cyan or yellow fluorescent proteins, CFP or YFP (SI Appendix, Fig.…”

“…Flagellar motility consumes several percent of total cellular protein and energy budget (9,10), which is primarily spent for the biogenesis of flagella and powering of their rotation, respectively, and to a lesser extent for the chemotactic signaling. Consistent with this high cost of motility, expression of flagellar genes can significantly reduce growth (11). Nevertheless, E. coli motility is up-regulated in poor carbon sources, as a part of the regulon controlled by cyclic adenosine monophosphate (cAMP) and its receptor protein (CRP) (1,12,13).…”

Evolution at the edge of expanding populations

“…Additional field examples of invasive populations, where margin individuals acquired greater dispersal and slower growth, include other plants (Ganeshaiah and Shaanker 1991;Huang et al 2015;Williams et al 2016), fish (Agostinho et al 2015), crickets (Simmons and Thomas 2004), butterflies (Hughes et al 2003), and fungi (Garbelotto et al 2015). Laboratory experiments with populations expanding towards a virgin territory with freshwater ciliates (Fronhofer and Altermatt 2015), beetles (Ochocki and Miller 2017;Weiss-Lehman et al 2017), plants (Williams et al 2016), and bacteria (Fraebel et al 2017;Ni et al 2017) led to similar results: population expansion can favor faster dispersal at the expense of slower growth.…”