Theory of chemotactic ring propagation and the fitness advantage of cue-driven range expansion

Many bacterial species are capable to sense and actively follow chemical gradients. For Escherichia coli, this chemotactic response belongs to the best-characterized subjects of molecular biology, but much less is known about its physiological function and fitness advantage. Previous studies have suggested chemotaxis as a foraging strategy under starvation conditions for which swimming is triggered as an emergency response to find new nutrient sources. However, this hypothesis has never been probed rigorously. Towards uncovering the physiological role of chemotaxis, we have systematically investigated the collective motion of cells along self-generated chemotactic gradients and its dependence on growth conditions*. Presenting experiments and a theoretical analysis, I discuss how the interplay of chemotactic sensing, proliferation, metabolite uptake, and swimming leads to the spreading and growth of an initially localized population. The collective migration dynamics of cells within ring-shaped fronts is described by a modified Keller-Segel model, emphasizing the crucial role of growth physiology and nutrient utilization. Coupled to the front propagation via pushed waves, proliferation of cells in the back drives overall population growth. As a consequence of the dynamics and the active regulation of motility genes, the speed of migration increases strongly with better growth conditions. By the integration of chemoattractant sensing into directed movement, the cue-driven form of range expansion described here is fast and easily outcompetes the canonical form of range-expansion via pulled waves and the Fisher-Kolmogorov dynamics. Overall, the results stand in strong contrast to the foraging hypothesis under starvation conditions but suggest the opposite: chemotaxis as an effective and foresighted strategy to optimize population growth and expansion when local conditions are good.
* with Tomyoa Honda, Ying Tang, Jeome Wong Ng, Massimo Vergassola, and Terence Hwa.