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 influx, which can burst the cell. To survive, cells rely on the passive response of mechanosensitive channels (Mscs), which open under increased membrane tension and allow the release of cytoplasmic solutes and water. Although the gating and the molecular structure of Mscs found in Escherichia coli have been extensively studied, the overall dynamics of the whole cell response remain poorly understood.

We present single-cell characterization of E. coli's passive response to a sudden downshock and show that initial fast volume expansion is followed by a slow volume recovery that can end below the initial value. Apart from the response of the wild type cells, we characterise the response of a double and hepta-mutant strain that lack all or some of the Mscs.

Finally, we present a theoretical model to explain the observations by simulating Mscs opening, solute efflux, and water flux. The model illustrates how solute efflux, driven by mechanical pressure and solute chemical potential, competes with water influx to reduce cellular osmotic pressure and allow volume recovery. It includes the stress stiffening characteristics of the cell wall and makes several predictions, which we discuss.