Optimal Cell Length for Exploration and Exploitation in Chemotactic Planktonic Bacteria

Elongated morphologies are prevalent among motile bacterioplankton in aquatic systems. This is often attributed to enhanced chemotactic ability, but how long is best? We hypothesized the existence of an optimal cell length for efficient chemotaxis resulting from shape-imposed physical constraints acting on the trade-off between rapid exploration versus efficient exploitation of nutrient sources. To test this hypothesis, we evaluated the chemotactic performance of elongated cephalexin-treated Escherichia coli towards α-methyl-aspartate in a microfluidic device creating linear, stable and quiescent chemical gradients. Our experiments showed cells of intermediate length aggregating most tightly to the chemoattractant source. A sensitivity analysis of an Individual-Based-Model replicating these results showed that 1) cells of intermediate length are optimal at transient states, whereas at steady state longest cells are best, 2) poor chemotactic performance of very short cells is caused by directionality loss, and 3) long cells are penalized by brief, slow runs. Finally, we evaluated chemotactic performance of cells of different length with simulations of a phycosphere, and found that long cells swimming in a run-and-reverse pattern with extended runs and moderate speeds are most efficient in this microenvironment. Overall, our results suggest that the stability of the chemical landscape plays a role in cell-size selection.