Elastic remodeling of model and cell membranes by rotating ATP synthase

Abstract

Energy homeostasis in cells relies on the rotary motion of ATP synthase. The spinning movement is also assumed to impact the mechanical properties of the surrounding lipids, leading to emergent effects such as non-equilibrium membrane fluctuations or protein curvature sorting in model systems. Here, we demonstrate that ATP synthase rotation reduces lateral pressure by decreasing lipid packing in both artificial and bacterial membranes. Using micropipette aspiration and fluorescence lifetime imaging microscopy, we find that the rotation of ATP synthase lowers the membrane tension of giant unilamellar vesicles, making the membranes more flexible. Fluorescent probes sensitive to lipid packing confirm that ATP synthase lowers membrane surface pressure during rotation. In vivo experiments in Bacillus subtilis further reveal that stimulation of ATP synthase rotation with specific drugs decreases the lateral pressure of the plasma membrane. These findings suggest that ATP synthase plays a significant role in modulating the mechanical properties of native membranes, potentially driving biological processes linked to membrane dynamics and protein self-assembly.