Escape band in Escherichia coli chemotaxis in opposing attractant and nutrient gradients

Abstract

Significance Not all nutrient molecules act as attractant signals, and not all attractants are good nutrients. Here, we study behaviors of bacterial cells in an environment with competing sources: One has a strong attractant but a poor nutrient, and the other has a rich nutrient but a weak attractant. We find that, although initially cells are attracted toward the strong attractant, the opposing nutrient gradient generated by consumption eventually becomes dominant when the cell density reaches a critical value. The cells then form a band escaping the strong attractant but weak nutrient “trap” and migrating toward the rich nutrient. Our study shows that combination of growth and chemotaxis allows cells to find nutrient source in complex environments with conflicting sensory cues. It is commonly believed that bacterial chemotaxis helps cells find food. However, not all attractants are nutrients, and not all nutrients are strong attractants. Here, by using microfluidic experiments, we studied Escherichia coli chemotaxis behavior in the presence of a strong chemoattractant (e.g., aspartate or methylaspartate) gradient and an opposing gradient of diluted tryptone broth (TB) growth medium. Our experiments showed that cells initially accumulate near the strong attractant source. However, after the peak cell density (h) reaches a critical value hc, the cells form a “escape band” (EB) that moves toward the chemotactically weaker but metabolically richer nutrient source. By using various mutant strains and varying experimental conditions, we showed that the competition between Tap and Tar receptors is the key molecular mechanism underlying the formation of the escape band. A mathematical model combining chemotaxis signaling and cell growth was developed to explain the experiments quantitatively. The model also predicted that the width w and the peak position xp of EB satisfy two scaling relations: w/l∼(h/hc)−1/2 and 1−xp/l∼(h/hc)−1/2, where l is the channel length. Both scaling relations were verified by experiments. Our study shows that the combination of nutrient consumption, population growth, and chemotaxis with multiple receptors allows cells to search for optimal growth condition in complex environments with conflicting sources.