The actin cytoskeleton is an active semi-flexible polymer network whose non-equilibrium properties coordinate both stable and contractile behaviors to maintain or change cell shape. While myosin motors drive the actin cytoskeleton out-of-equilibrium, the role of myosin-driven active stresses in the accumulation and dissipation of mechanical energy is unclear. To investigate this, we synthesize an actomyosin material in vitro whose active stress content can tune the network from stable to contractile. Each increment in activity determines a characteristic spectrum of actin filament fluctuations which is used to calculate the total mechanical work and the production of entropy in the material. We find that the balance of work and entropy does not increase monotonically and the entropy production rate is maximized in the non-contractile, stable state of actomyosin. Our study provides evidence that the origins of entropy production and activity-dependent dissipation relate to disorder in the molecular interactions between actin and myosin.
Active stresses are generated and transmitted throughout diverse F-actin architectures within the cell cytoskeleton, and drive essential behaviors of the cell, from cell division to migration. However, while the impact of F-actin architecture on the transmission of stress is well studied, the role of architecture on the ab initio generation of stresses remains less understood. Here, we assemble F-actin networks in vitro, whose architectures are varied from branched to bundled through F-actin nucleation via Arp2/3 and the formin mDia1. Within these architectures, we track the motions of embedded myosin thick filaments and connect them to the extent of F-actin network deformation. While mDia1-nucleated networks facilitate the accumulation of stress and drive contractility through enhanced actomyosin sliding, branched networks prevent stress accumulation through the inhibited processivity of thick filaments. The reduction in processivity is due to a decrease in translational and rotational motions constrained by the local density and geometry of F-actin.
Essentially all biology is active and dynamic. Biological entities autonomously sense, compute, and respond using energy-coupled ratchets that can produce force and do work. The cytoskeleton, along with its associated proteins and motors, is a canonical example of biological active matter, which is responsible for cargo transport, cell motility, division, and morphology. Prior work on cytoskeletal active matter systems showed either extensile or contractile dynamics. Here, we demonstrate a cytoskeletal system that can control the direction of the network dynamics to be either extensile, contractile, or static depending on the concentration of filaments or transient crosslinkers through systematic variation of the crosslinker or microtubule concentrations. Based off these new observations and our previously published results, we created a simple one-dimensional model of the interaction of filaments within a bundle. Despite its simplicity, our model recapitulates the observed activities of our experimental system, implying that the dynamics of our finite networks of bundles are driven by the local filament-filament interactions within the bundle. Finally, we show that contractile phases can result in autonomously motile networks that resemble cells. Our experiments and model allow us to gain a deeper understanding of cytoskeletal dynamics and provide a stepping stone for designing active, autonomous systems that could potentially dynamically switch states.
Incorporating growth into contemporary material functionality presents a grand challenge in materials design. The F-actin cytoskeleton is an active polymer network that serves as the mechanical scaffolding for eukaryotic cells, growing and remodeling in order to determine changes in cell shape. Nucleated from the membrane, filaments polymerize and grow into a dense network whose dynamics of assembly and disassembly, or "turnover," coordinates both fluidity and rigidity. Here, the extent of F-actin nucleation is varied from a membrane surface in a biomimetic model of the cytoskeleton constructed from purified protein. It is found that nucleation of F-actin mediates the accumulation and dissipation of polymerization-induced F-actin bending energy. At high and low nucleation, bending energies are low and easily relaxed yielding an isotropic material. However, at an intermediate critical nucleation, stresses are not relaxed by turnover and the internal energy accumulates 100-fold. In this case, high filament curvatures template further assembly of F-actin, driving the formation and stabilization of vortexlike topological defects. Thus, nucleation coordinates mechanical and chemical timescales to encode shape memory into active materials.
We investigate ordering of granular rods in a container subject to vibrations in a gravitational field as a function of number density of the rods. We study rods with three different length to diameter aspect ratios A(r)= 5, 10, and 15. The measurements are performed in three dimensions using x-ray computer tomography to visualize the rods in the entire container. We first discuss a method to extract the position and orientation of the rods from the scans which enables us to obtain statistical measures of the degree of order in the packing. We find that the rods with A(r)=5 phase separate into domains with vertical and horizontal orientation as the number density of the rods is increased, whereas, for A(r)=10 and 15 the rods are predominately oriented vertically in layers. By calculating two-point spatial correlation functions, we further show that long range hexagonal order occurs within a layer when the rods are oriented along the vertical axis. Thus, our experiments find that long range order increases rapidly in granular rods with growing anisotropy.
We investigate the effect of shape anisotropy and number density on the dynamics of granular rods on a substrate with experiments using a mono-layer of bead chains in a vibrated container. Statistical measures of the translational and rotational degrees of freedom indicate a dramatic slowing down of dynamics because of steric interactions at a value well below the highest packing fraction of the chains. In particular, the in-plane orientation auto-correlation function decays exponentially with time at low densities, but increasingly slowly as density is increased with a form which is not described by a simple exponential function. While the mean square displacement of the chain center of mass is observed to grow linearly at low densities, it is observed to grow increasingly slowly and non-linearly as number density is increased. Decomposing the displacements parallel and perpendicular to the long axis of the chain, we find that the ratio of diffusion in the parallel and perpendicular direction to their long axis is less than one in the dilute regime. However, as the density of the chains is increased, the ratio rapidly increases above one with a greater value for higher aspect ratios. This anisotropic behavior can be explained by considering a higher effective drag on the rods by the substrate in the perpendicular direction compared with the parallel direction, and by tube-like dynamics at higher densities.
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