Abstract
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.
Highlights
Bacteria and Eukaryotic cells must resist mechanical forces when they bind to their surroundings
Cells adhere to surfaces and each other in the presence of forces that would 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
Type 1 fimbriae provide and ideal system for understanding the role of tether elasticity in dynamic cell adhesion. This would require methods to probe the forces on single fimbriae during dynamic cell adhesion, and to change fimbrial elastic properties
Summary
Bacteria and Eukaryotic cells must resist mechanical forces when they bind to their surroundings. Bacteria and blood cells adhere to other cells or tissues in the presence of fluid flow that applies a drag force on the cell, while many other cells apply force to each other or to solid surfaces via cytoskeletal contraction. These mechanical forces affect the lifetime of the individual noncovalent receptor-ligand bonds that mediate cell adhesion. Strong and stable cell adhesion requires clusters with multiple receptor-ligand bonds. This raises the question of whether cells have evolved mechanisms of stabilizing bond clusters
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