Evolutionary Remodeling of Bacterial Motility Checkpoint Control

Regulatory 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. [Display omitted] •Multiple mutations enhance swimming behavior under selection•A universal trade-off relationship between motility and growth is observed•Checkpoint remodeling provides a mechanism of evolutionary adaptation•Bow-tie topology facilitates evolvability of the motility network Ni et al. use experimental evolution to investigate remodeling of bacterial motility under selection. Their study reveals a key role of the checkpoint control of flagellar gene expression in motility evolution. Bow-tie topology of the checkpoint control facilitates evolutionary tuning of the trade-off between motility and growth.