Optimal cell length for exploration and exploitation in chemotactic planktonic bacteria

Abstract

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 first evaluated the chemotactic performance of elongated cephalexin-treated Escherichia coli towards -methyl-aspartate in an agarose-based microfluidic device that creates linear, stable and quiescent chemical gradients. Our experiments showed that cells of intermediate lengths aggregated most tightly to the chemoattractant source. We then replicated these experimental results with Individual Based Model (IBM) simulations. A sensitivity analysis of the IBM allowed us to gain mechanistic insights into which parameters drive this trend and showed that the poor chemotactic performance of very short cells is caused by loss of directionality, whereas long cells are penalized by brief, slow runs. Finally, we evaluated the chemotactic performance of cells of different length with IBM simulations of a phycosphere - a hotspot of microbial interactions in the ocean. Results indicated that long cells swimming in a run-and-reverse pattern with extended runs and moderate speeds are most efficient at harvesting nutrients in this microenvironment. The combination of microfluidic experiments and IBMs proves thus to be a powerful tool for untangling the physical constraints that motile bacteria are facing in aquatic systems.