Dynamics of Escherichia coli's passive response to a sudden decrease in external osmolarity

For most cells, a sudden decrease in external osmolarity results in fast water inux that can burst the cell. To survive, cells rely on the passive response of mechanosensitive channels, which open under increased membrane tension and allow the release of cytoplasmic solutes and water. Although the gating and the molecular structure of mechanosensitive channels found in Escherichia coli have been extensively studied, the overall dynamics of the whole cellular response remain poorly understood. Here we characterize E. coli's passive response to a sudden hypo-osmotic shock (downshock) on a single-cell level. We show that initial fast volume expansion is followed by a slow volume recovery that can end below the initial value. Similar response patterns were observed at downshocks of a wide range of magnitudes. While wild type cells adapted to osmotic downshocks and resumed growing, cells of a double mutant (ΔmscLΔmscS) strain expanded, but failed to fully recover, often lysing or not resuming growth at high osmotic downshocks. We propose a theoretical model to explain our observations by simulating mechanosensitive channels opening, and subsequent solute efflux and water flux. The model illustrates how solute effluux, driven by mechanical pressure and solute chemical potential, competes with water inux to reduce cellular osmotic pressure and allow volume recovery. Our work highlights the vital role of mechanosensation in bacterial survival.