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Peeling dynamics of fluid membranes bridged by molecular bonds: moving or breaking

Biological adhesion is a critical mechanical function of complex organisms operating at multiple scales. At the cellular scale, cell-cell adhesion is remarkably tunable to enable both cohesion and malleability during development, homeostasis and disease. Such adaptable adhesion is physically supported by transient bonds between laterally mobile molecules embedded in fluid membranes. Thus, unlike specific adhesion at solid-solid or solid-fluid interfaces, peeling at fluid-fluid interfaces can proceed by breaking bonds, by moving bonds, or by a combination of both. How the additional degree of freedom provided by bond mobility changes the mechanics of peeling is not understood. To address this, we develop a theoretical model coupling self-consistently diffusion, reactions and mechanics. Lateral mobility and reaction rates determine distinct peeling regimes. In a diffusion-dominated Stefan-like regime, bond motion establishes self-stabilizing dynamics that increase the effective adhesion fracture energy. A reaction-dominated regime exhibits traveling peeling solutions where small-scale diffusion and marginal unbinding control peeling speed. In a mixed reaction-diffusion regime, strengthening by bond motion competes with weakening by bond breaking in a force-dependent manner, defining the strength of the adhesion patch. In turn, patch strength depends on molecular properties such as bond stiffness, force sensitivity, or crowding. We thus establish the physical rules enabling tunable cohesion in cellular tissues and in engineered biomimetic systems.