Dissecting Molecular Origins of the Mechano-Adaptive Behaviors of Actomyosin Bundles

Actomyosin bundles, composed mainly of actin filaments, myosin II filaments, and actin cross-linking proteins, are central to force generation and maintenance in non-striated muscle cells. Actomyosin bundles exhibit diverse mechano-adaptive responses to external mechanical cues. However, the molecular mechanisms underlying such adaptability remain poorly understood. In this study, we employed experiments and agent-based simulations to illuminate how actomyosin bundles adapt to complex mechanical perturbations. Our experiments revealed that individual stress fibers isolated from cells, and thus operating independently of cellular regulation, exhibited buckling in response to rapid compressions following stretch, accompanied by gradual recovery to a straight configuration. Such buckling was not observed under slow compression, indicating that the bundles exhibit rate-dependent adaptive responses. These findings demonstrate that mechano-adaptive behavior is an intrinsic property of actomyosin bundles. Simulations successfully reproduced these rate-dependent behaviors intrinsic to actomyosin bundles and identified key factors determining the dependence. Bundle stiffness influenced the buckling-induced curvature but had little effect on the time required for recovery to straight configuration. Motor density did not alter the recovery time but significantly influenced the magnitude of tensile forces developed after full recovery. The recovery time was primarily governed by the motor walking rate and the applied compressive strain rate. This work reveals how intrinsic mechanics and motor activity drive actomyosin bundle behavior in cellular mechano-adaptation.