Coordination of gene expression with cell size enables Escherichia coli to efficiently maintain motility across conditions

Abstract

To swim and navigate, motile bacteria synthesize a complex motility machinery involving flagella, motors, and a sensory system. A myriad of studies has elucidated the molecular processes involved, but less is known about the coordination of motility expression with cellular physiology: In Escherichia coli, motility genes are strongly upregulated in nutrient-poor conditions compared to nutrient-replete conditions; yet a quantitative link to cellular motility has not been developed. Here, we systematically investigate gene expression, swimming behavior, and cell growth across a broad spectrum of exponential growth condition. We establish that E. coli up-regulates the expression of motility genes at slow growth to compensate for reduction in cell size, such that the number of flagella per cell is maintained across conditions. The observed 4-5 flagella per cell is the minimum number needed to keep the majority of cells motile. This simple regulatory objective allows E. coli cells to remain motile across a broad range of growth conditions while keeping the biosynthetic and energetic demands to establish and drive the motility machinery at the minimum needed. Given the strong reduction in flagella synthesis resulting from cell size increases at fast growth, our findings also provide a novel physiological perspective on bacterial cell size control: A larger cell-size at fast growth is an efficient strategy to increase the allocation of cellular resources to the synthesis of those proteins required for fast growth, while maintaining processes such as motility which are only needed on a per-cell basis.