Bacterial cell lysis: geometry, elasticity, and implications

Membrane lysis, or rupture, is a cell death pathway in bacteria frequently caused by cell wall-targeting antibiotics. Although several studies have clarified biochemical mechanisms of antibiotic action, a physical understanding of the processes leading to lysis remains lacking. Here, we analyze the dynamics of membrane bulging and lysis in Escherichia coli, where, strikingly, the formation of an initial bulge (\"bulging\") after cell wall digestion occurs on a characteristic timescale as fast as 100 ms and the growth of the bulge (\"swelling\") occurs on a slower characteristic timescale of 10-100 s. We show that bulging can be energetically favorable due to the relaxation of the entropic and stretching energies of the inner membrane, cell wall, and outer membrane and that experimentally observed bulge shapes are consistent with model predictions. We then show that swelling can involve both the continued flow of water into the cytoplasm and the enlargement of wall defects, after which cell lysis is consistent with both the inner and outer membranes exceeding characteristic estimates of the yield areal strains of biological membranes. Our results contrast biological membrane physics and the physics of thin shells, reveal principles of how all bacteria likely function in their native states, and may have implications for cellular morphogenesis and antibiotic discovery across different species of bacteria.