Simulations of dynamically cross-linked actin networks: Morphology, rheology, and hydrodynamic interactions

Cross-linked actin networks are the primary component of the cell cytoskeleton and have been the subject of numerous experimental and modeling studies. While these studies have demonstrated that the networks are viscoelastic materials, evolving from elastic solids on short timescales to viscous fluids on long ones, questions remain about the duration of each asymptotic regime, the role of the surrounding fluid, and the behavior of the networks on intermediate timescales. Here we perform detailed simulations of passively cross-linked non-Brownian actin networks to quantify the principal timescales involved in the elastoviscous behavior, study the role of nonlocal hydrodynamic interactions, and parameterize continuum models from discrete stochastic simulations. To do this, we extend our recent computational framework for semiflexible filament suspensions, which is based on nonlocal slender body theory, to actin networks with dynamic cross linkers and finite filament lifetime. We introduce a model where the cross linkers are elastic springs with sticky ends stochastically binding to and unbinding from the elastic filaments, which randomly turn over at a characteristic rate. We show that, depending on the parameters, the network evolves to a steady state morphology that is either an isotropic actin mesh or a mesh with embedded actin bundles. For different degrees of bundling, we numerically apply small-amplitude oscillatory shear deformation to extract three timescales from networks of hundreds of filaments and cross linkers. We analyze the dependence of these timescales, which range from the order of hundredths of a second to the actin turnover time of several seconds, on the dynamic nature of the links, solvent viscosity, and filament bending stiffness. We show that the network is mostly elastic on the short time scale, with the elasticity coming mainly from the cross links, and viscous on the long time scale, with the effective viscosity originating primarily from stretching and breaking of the cross links. We show that the influence of nonlocal hydrodynamic interactions depends on the network morphology: for homogeneous meshworks, nonlocal hydrodynamics gives only a small correction to the viscous behavior, but for bundled networks it both hinders the formation of bundles and significantly lowers the resistance to shear once bundles are formed. We use our results to construct three-timescale generalized Maxwell models of the networks.

Phoretic self-propulsion of helical active particles

Chemically active colloids self-propel by catalysing the decomposition of molecular ‘fuel’ available in the surrounding solution. If the various molecular species involved in the reaction have distinct interactions with the colloid surface, and if the colloid has some intrinsic asymmetry in its surface chemistry or geometry, there will be phoretic flows in an interfacial layer surrounding the particle, leading to directed motion. Most studies of chemically active colloids have focused on spherical, axisymmetric ‘Janus’ particles, which (in the bulk, and in absence of fluctuations) simply move in a straight line. For particles with a complex (non-spherical and non-axisymmetric) geometry, the dynamics can be much richer. Here, we consider chemically active helices. Via numerical calculations and slender body theory, we study how the translational and rotational velocities of the particle depend on geometry and the distribution of catalytic activity over the particle surface. We confirm the recent finding of Katsamba et al. (J. Fluid Mech., vol. 898, 2020, p. A24) that both tangential and circumferential concentration gradients contribute to the particle velocity. The relative importance of these contributions has a strong impact on the motion of the particle. We show that, by a judicious choice of the particle design parameters, one can suppress components of angular velocity that are perpendicular to the screw axis, or even select for purely ‘sideways’ translation of the helix.

Regularized Stokeslets Lines Suitable for Slender Bodies in Viscous Flow

Slender-body approximations have been successfully used to explain many phenomena in low-Reynolds number fluid mechanics. These approximations typically use a line of singularity solutions to represent flow. These singularities can be difficult to implement numerically because they diverge at their origin. Hence, people have regularized these singularities to overcome this issue. This regularization blurs the force over a small blob and thereby removing divergent behaviour. However, it is unclear how best to regularize the singularities to minimize errors. In this paper, we investigate if a line of regularized Stokeslets can describe the flow around a slender body. This is achieved by comparing the asymptotic behaviour of the flow from the line of regularized Stokeslets with the results from slender-body theory. We find that the flow far from the body can be captured if the regularization parameter is proportional to the radius of the slender body. This is consistent with what is assumed in numerical simulations and provides a choice for the proportionality constant. However, more stringent requirements must be placed on the regularization blob to capture the near field flow outside a slender body. This inability to replicate the local behaviour indicates that many regularizations cannot satisfy the no-slip boundary conditions on the body’s surface to leading order, with one of the most commonly used blobs showing an angular dependency of velocity along any cross section. This problem can be overcome with compactly supported blobs, and we construct one such example blob, which can be effectively used to simulate the flow around a slender body.

Remarks on Regularized Stokeslets in Slender Body Theory

We remark on the use of regularized Stokeslets in the slender body theory (SBT) approximation of Stokes flow about a thin fiber of radius ϵ>0. Denoting the regularization parameter by δ, we consider regularized SBT based on the most common regularized Stokeslet plus a regularized doublet correction. Given sufficiently smooth force data along the filament, we derive L∞ bounds for the difference between regularized SBT and its classical counterpart in terms of δ, ϵ, and the force data. We show that the regularized and classical expressions for the velocity of the filament itself differ by a term proportional to log(δ/ϵ); in particular, δ=ϵ is necessary to avoid an O(1) discrepancy between the theories. However, the flow at the surface of the fiber differs by an expression proportional to log(1+δ2/ϵ2), and any choice of δ∝ϵ will result in an O(1) discrepancy as ϵ→0. Consequently, the flow around a slender fiber due to regularized SBT does not converge to the solution of the well-posed slender body PDE which classical SBT is known to approximate. Numerics verify this O(1) discrepancy but also indicate that the difference may have little impact in practice.

Simulations of dynamically cross-linked actin networks: morphology, rheology, and hydrodynamic interactions

Cross-linked actin networks are the primary component of the cell cytoskeleton and have been the subject of numerous experimental and modeling studies. While these studies have demonstrated that the networks are viscoelastic materials, evolving from elastic solids on short timescales to viscous fluids on long ones, questions remain about the duration of each asymptotic regime, the role of the surrounding fluid, and the behavior of the networks on intermediate timescales. Here we perform detailed simulations of passively cross-linked actin networks to quantify the principal timescales involved in the elastoviscous behavior, study the role of nonlocal hydrodynamic interactions, and derive continuum models from discrete stochastic simulations. To do this, we extend our recent computational framework for semiflexible filament suspensions, which is based on nonlocal slender body theory, to actin networks with dynamic cross linkers. We introduce a model where the cross linkers are elastic springs with sticky ends stochastically binding to and unbinding from the elastic filaments, which randomly turn over at a characteristic rate. We show that, depending on the parameters, the network evolves to a steady state morphology that is either an isotropic actin mesh or a mesh with embedded actin bundles. For different degrees of bundling, we numerically apply small-amplitude oscillatory shear deformation to extract three timescales from networks of hundreds of filaments and cross linkers. We analyze the dependence of these timescales, which range from the order of hundredths of a second to several seconds, on the dynamic nature of the links, solvent viscosity, and filament bending stiffness. We show that the network is mostly elastic on the short time scale, with the elasticity coming mainly from the cross links, and viscous on the long time scale, with the effective viscosity originating primarily from stretching and breaking of the cross links. We show that the influence of nonlocal hydrodynamic interactions depends on the network morphology: for homogeneous meshworks, nonlocal hydrodynamics gives only a small correction to the viscous behavior, but for bundled networks it both hinders the formation of bundles and significantly lowers the resistance to shear once bundles are formed. We use our results to construct continuum Maxwell-type models of the networks.

Hydrodynamic interactions are key in thrust-generation of microswimmers with hairy flagella

The important role of flagellates in aquatic microbial food webs is mediated by their flagella that enable them to swim and generate a feeding current. The flagellum in most predatory flagellates is equipped with rigid hairs that reverse the direction of thrust compared to the thrust due to a smooth flagellum. Conventionally, such reversal has been attributed to drag anisotropy of individual hairs, neglecting their hydrodynamic interactions. Here, we show that hydrodynamic interactions are key to thrust-generation and reversal in hairy flagellates, making their hydrodynamics fundamentally different from the slender-body theory governing microswimmers with smooth flagella. Using computational fluid dynamics and model analysis, we demonstrate that long and not too closely spaced hairs and strongly curved flagellar waveforms are optimal for thrust-generation. Our results form a theoretical basis for understanding the diverse flagellar architectures and feeding modes found in predatory flagellates.

Control of Uniflagellar Soft Robots at Low Reynolds Number Using Buckling Instability

In this paper, we analyze the inverse dynamics and control of a bacteria-inspired uniflagellar robot in a fluid medium at low Reynolds number. Inspired by the mechanism behind the locomotion of flagellated bacteria, we consider a robot comprising a flagellum—a flexible helical filament—connected to a spherical head. The flagellum rotates about the head at a controlled angular velocity and generates a propulsive force that moves the robot forward. When the angular velocity exceeds a threshold value, the hydrodynamic force exerted by the fluid can cause the soft flagellum to buckle, characterized by a dramatic change in its shape. In this computational study, a fluid–structure interaction model that combines Discrete Elastic Rods algorithm with Lighthill's Slender Body Theory is employed to simulate the locomotion and deformation of the robot. We demonstrate that the robot can follow a prescribed path in three-dimensional space by exploiting buckling of the flagellum. The control scheme involves only a single (binary) scalar input—the angular velocity of the flagellum. By triggering the buckling instability at the right moment, the robot can follow the path in three-dimensional space. We also show that the complexity of the dynamics of the helical filament can be captured using a deep neural network, from which we identify the input–output functional relationship between the control input and the trajectory of the robot. Furthermore, our study underscores the potential role of buckling in the locomotion of natural bacteria.