Electrochemical gradients across biological membranes are fundamental to cellular bioenergetics. In bacteria, the proton motive force (PMF) drives critical functions such as ATP synthesis and motility. Although historically regarded as temporally and spatially stable, recent studies have revealed dynamic PMF behaviors at single-cell and community levels, which are implicated in processes like intracellular communication and coordination. The bacterial flagellar motor, a rotary nanomachine directly powered by the PMF, provides a unique and sensitive tool for probing these dynamics. By employing light-activated proton pumps and monitoring changes in flagellar motor activity, we perturb and investigate the PMF at the single-cell level. This approach reveals millisecond-scale temporal fluctuations and rapid lateral homogenization of the PMF, reminiscent of the electrotonic potential spread observed in passive neurons.