Microorganisms often move through viscoelastic environments, as biological fluids frequently have a rich microstructure owing to the presence of large polymeric molecules. Research on the effect of fluid elasticity on the swimming kinematics of these organisms has usually been focused on those that move via cilia or flagellum. Experimentally, Shen (X. N. Shen et al. , Phys. Rev. Lett. , 2011, 106 , 208101) reported that the nematode C. elegans , a model organism used to study undulatory motion, swims more slowly as the Deborah number describing the fluid's elasticity is increased. This phenomenon has not been thoroughly studied via a fully resolved three-dimensional simulation; moreover, the effect of fluid elasticity on the swimming speed of organisms moving via euglenoid movement, such as E. gracilis , is completely unknown. In this study, we discuss the simulation of the arbitrary motion of an undulating or pulsating swimmer that occupies finite volume in three dimensions, with the ability to specify any differential viscoelastic rheological model for the surrounding fluid. To accomplish this task, we use a modified version of the Immersed Finite Element Method presented in a previous paper by Guido and Saadat in 2018 (A. Saadat et al. , Phys. Rev. E , 2018, 98 , 063316). In particular, this version allows for the simulation of deformable swimmers such that they evolve through an arbitrary set of specified shapes via a conformation-driven force. From our analysis, we observe several key trends not found in previous two-dimensional simulations or theoretical analyses for C. elegans , as well as novel results for the amoeboid motion. In particular, we find that regions of high polymer stress concentrated at the head and tail of the swimming C. elegans are created by strong extensional flow fields and are associated with a decrease in swimming speed for a given swimming stroke. In contrast, in two dimensions these regions of stress are commonly found distributed along the entire body, likely owing to the lack of a third dimension for polymer relaxation. A comparison of swim speeds shows that the calculations in two-dimensional simulations result in an over-prediction of the speed reduction. We believe that our simulation tool accurately captures the swimming motion of the two aforementioned model swimmers and furthermore, allows for the simulation of multiple deformable swimmers, as well as more complex swimming geometries. This methodology opens many new possibilities for future studies of swimmers in viscoelastic fluids.
more »
« less
Performance of a Helical Microswimmer Traversing a Discrete Viscoelastic Network with Dynamic Remodeling
Microorganisms often navigate a complex environment composed of a viscous fluid with suspended microstructures such as elastic polymers and filamentous networks. These microstructures can have similar length scales to the microorganisms, leading to complex swimming dynamics. Some microorganisms secrete enzymes that dynamically change the elastic properties of the viscoelastic networks through which they move. In addition to biological organisms, microrobots have been engineered with the goals of mucin gel penetration or dissolving blood clots. In order to gain insight into the coupling between swimming performance and network remodeling, we used a regularized Stokeslet boundary element method to compute the motion of a microswimmer consisting of a rotating spherical body and counter-rotating helical flagellum. The viscoelastic network is represented by a network of points connected by virtual elastic linkages immersed in a viscous fluid. Here, we model the enzymatic dissolution of the network by bacteria or microrobots by dynamically breaking elastic linkages when the cell body of the swimmer falls within a given distance from the link. We investigate the swimming performance of the microbes as they penetrate and move through networks of different material properties, and also examine the effect of network remodeling.
more »
« less
- Award ID(s):
- 1951707
- NSF-PAR ID:
- 10412980
- Date Published:
- Journal Name:
- Fluids
- Volume:
- 7
- Issue:
- 8
- ISSN:
- 2311-5521
- Page Range / eLocation ID:
- 257
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Microorganisms are commonly found swimming in complex biological fluids such as mucus and these fluids respond elastically to deformation. These viscoelastic fluids have been previously shown to affect the swimming kinematics of these microorganisms in non-trivial ways depending on the rheology of the fluid, the particular swimming gait and the structural properties of the immersed body. In this report we put forth a previously unmentioned mechanism by which swimming organisms can experience a speed increase in a viscoelastic fluid. Using numerical simulations and asymptotic theory we find that significant swirling flow around a microscopic swimmer couples with the elasticity of the fluid to generate a marked increase in the swimming speed. We show that the speed enhancement is related to the introduction of mixed flow behind the swimmer and the presence of hoop stresses along its body. Furthermore, this effect persists when varying the fluid rheology and when considering different swimming gaits. This, combined with the generality of the phenomenon (i.e. the coupling of vortical flow with fluid elasticity near a microscopic swimmer), leads us to believe that this method of speed enhancement could be present for a wide range of microorganisms moving through complex fluids.more » « less
-
Merks, Roeland M.H. (Ed.)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.more » « less
-
The development of novel drug delivery systems, which are revolutionizing modern medicine, is benefiting from studies on microorganisms’ swimming. In this paper we consider a model microorganism (a squirmer) enclosed in a viscous droplet to investigate the effects of medium heterogeneity or geometry on the propulsion speed of the caged squirmer. We first consider the squirmer and droplet to be spherical (no shape effects) and derive exact solutions for the equations governing the problem. For a squirmer with purely tangential surface velocity, the squirmer is always able to move inside the droplet (even when the latter ceases to move as a result of large fluid resistance of the heterogeneous medium). Adding radial modes to the surface velocity, we establish a new condition for the existence of a co-swimming speed (where squirmer and droplet move at the same speed). Next, to probe the effects of geometry on propulsion, we consider the squirmer and droplet to be in Newtonian fluids. For a squirmer with purely tangential surface velocity, numerical simulations reveal a strong dependence of the squirmer's speed on shapes, the size of the droplet and the viscosity contrast. We found that the squirmer speed is largest when the droplet size and squirmer's eccentricity are small, and the viscosity contrast is large. For co-swimming, our results reveal a complex, non-trivial interplay between the various factors that combine to yield the squirmer's propulsion speed. Taken together, our study provides several considerations for the efficient design of future drug delivery systems.more » « less
-
The mechanical properties of the cell nucleus are increasingly recognized as critical in many biological processes. The deformability of the nucleus determines the ability of immune and cancer cells to migrate through tissues and across endothelial cell layers, and changes to the mechanical properties of the nucleus can serve as novel biomarkers in processes such as cancer progression and stem cell differentiation. However, current techniques to measure the viscoelastic nuclear mechanical properties are often time consuming, limited to probing one cell at a time, or require expensive, highly specialized equipment. Furthermore, many current assays do not measure time-dependent properties, which are characteristic of viscoelastic materials. Here, we present an easy-to-use microfluidic device that applies the well-established approach of micropipette aspiration, adapted to measure many cells in parallel. The device design allows rapid loading and purging of cells for measurements, and minimizes clogging by large particles or clusters of cells. Combined with a semi-automated image analysis pipeline, the microfluidic device approach enables significantly increased experimental throughput. We validated the experimental platform by comparing computational models of the fluid mechanics in the device with experimental measurements of fluid flow. In addition, we conducted experiments on cells lacking the nuclear envelope protein lamin A/C and wild-type controls, which have well-characterized nuclear mechanical properties. Fitting time-dependent nuclear deformation data to power law and different viscoelastic models revealed that loss of lamin A/C significantly altered the elastic and viscous properties of the nucleus, resulting in substantially increased nuclear deformability. Lastly, to demonstrate the versatility of the devices, we characterized the viscoelastic nuclear mechanical properties in a variety of cell lines and experimental model systems, including human skin fibroblasts from an individual with a mutation in the lamin gene associated with dilated cardiomyopathy, healthy control fibroblasts, induced pluripotent stem cells (iPSCs), and human tumor cells. Taken together, these experiments demonstrate the ability of the microfluidic device and automated image analysis platform to provide robust, high throughput measurements of nuclear mechanical properties, including time-dependent elastic and viscous behavior, in a broad range of applications.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/fluids7080257
