Yielding Elastic Tethers Stabilize Robust Cell Adhesion

Many bacteria and eukaryotic cells express adhesive proteins at the end of tethers that elongate reversibly at constant or near constant force, which we refer to as yielding elasticity. Here we address the function of yielding elastic adhesive tethers with Escherichia coli bacteria as a model for cell adhesion, using a combination of experiments and simulations. The adhesive bond kinetics and tether elasticity was modeled in the simulations with realistic biophysical models that were fit to new and previously published single molecule force spectroscopy data. The simulations were validated by comparison to experiments measuring the adhesive behavior of E. coli in flowing fluid. Analysis of the simulations demonstrated that yielding elasticity is required for the bacteria to remain bound in high and variable flow conditions, because it allows the force to be distributed evenly between multiple bonds. In contrast, strain-hardening and linear elastic tethers concentrate force on the most vulnerable bonds, which leads to failure of the entire adhesive contact. Load distribution is especially important to noncovalent receptor-ligand bonds, because they become exponentially shorter lived at higher force above a critical force, even if they form catch bonds. The advantage of yielding is likely to extend to any blood cells or pathogens adhering in flow, or to any situation where bonds are stretched unequally due to surface roughness, unequal native bond lengths, or conditions that act to unzip the bonds. Author Summary: Cells adhere to surfaces and each other in the presence of forces that would easily overpower the individual noncovalent receptor-ligand bonds that mediate this adhesion, raising the question as to how these bonds cooperate to withstand such high forces. Here we show that cooperation and robust adhesion depends on the elastic properties of the bonds. A type of nonlinear elasticity referred to as elastic yielding ensures that the total force is distributed equally across the individual bonds regardless of geometry. In contrast, with linear or strain-hardening elasticity, the bonds that are stretched the most are exposed to higher forces, which cause them to fail sequentially. This work explains why elastic yielding is found in structurally and evolutionarily diverse adhesive complexes.