Interactions between swimming cells and surfaces are essential to many microbiological processes, from bacterial biofilm formation to human fertilization. However, despite their fundamental importance, relatively little is known about the physical mechanisms that govern the scattering of flagellated or ciliated cells from solid surfaces. A more detailed understanding of these interactions promises not only new biological insights into structure and dynamics of flagella and cilia but may also lead to new microfluidic techniques for controlling cell motility and microbial locomotion, with potential applications ranging from diagnostic tools to therapeutic protein synthesis and photosynthetic biofuel production. Due to fundamental differences in physiology and swimming strategies, it is an open question of whether microfluidic transport and rectification schemes that have recently been demonstrated for pusher-type microswimmers such as bacteria and sperm cells, can be transferred to pullertype algae and other motile eukaryotes, because it is not known whether long-range hydrodynamic or short-range mechanical forces dominate the surface interactions of these microorganisms. Here, using high-speed microscopic imaging, we present direct experimental evidence that the surface scattering of both mammalian sperm cells and unicellular green algae is primarily governed by direct ciliary contact interactions. Building on this insight, we predict and experimentally verify the existence of optimal microfluidic ratchets that maximize rectification of initially uniform Chlamydomonas reinhardtii suspensions. Because mechano-elastic properties of cilia are conserved across eukaryotic species, we expect that our results apply to a wide range of swimming microorganisms.algal surface accumulation | swimming rectification S urface interactions of motile cells play crucial roles in a wide range of microbiological phenomena, perhaps most prominently in the formation of biofilms (1) and during the fertilization of mammalian ova (2). However, despite their widely recognized importance, the basic physical mechanisms that govern the response of swimming bacteria, algae, or spermatozoa to solid surfaces have remained unclear. This predicament is exemplified by the current debate (3-6) about the relevance of hydrodynamic long-range forces and steric short-range interactions for the accumulation of flagellated cells at liquid-solid interfaces. From a general perspective, improving our understanding of cell surface scattering processes promises not only new insights into structure, dynamics, and biological functions of flagella and cilia, it will also help to advance microfluidic techniques for controlling microbial locomotion (7,8), with potential applications in diagnostics (9), therapeutic protein synthesis (10), and photosynthetic biofuel production (11-14). That microfluidic circuits provide an excellent test bed for developing and assessing new strategies for the control of cell motility was recently demonstrated by the rectification of ...
A major puzzle in biology is how mammalian sperm maintain the correct swimming direction during various phases of the sexual reproduction process. Whilst chemotaxis may dominate near the ovum, it is unclear which cues guide spermatozoa on their long journey towards the egg. Hypothesized mechanisms range from peristaltic pumping to temperature sensing and response to fluid flow variations (rheotaxis), but little is known quantitatively about them. We report the first quantitative study of mammalian sperm rheotaxis, using microfluidic devices to investigate systematically swimming of human and bull sperm over a range of physiologically relevant shear rates and viscosities. Our measurements show that the interplay of fluid shear, steric surface-interactions, and chirality of the flagellar beat leads to stable upstream spiralling motion of sperm cells, thus providing a generic and robust rectification mechanism to support mammalian fertilisation. A minimal mathematical model is presented that accounts quantitatively for the experimental observations.DOI: http://dx.doi.org/10.7554/eLife.02403.001
Experimental results on the tank-treading-tumbling transition in the dynamics of a vesicle subjected to a shear flow as a function of a vesicle excess area, viscosity contrast, and the normalized shear rate are presented. Good agreement on the transition curve and scaling behavior with theory and numerical simulations was found. A new type of unsteady motion at a large degree of vesicle deformability was discovered and described as follows: a vesicle trembles around the flow direction, while the vesicle shape strongly oscillates.
The migratory abilities of motile human spermatozoa in vivo are essential for natural fertility, but it remains a mystery what properties distinguish the tens of cells which find an egg from the millions of cells ejaculated. To reach the site of fertilization, sperm must traverse narrow and convoluted channels, filled with viscous fluids. To elucidate individual and group behaviors that may occur in the complex three-dimensional female tract environment, we examine the behavior of migrating sperm in assorted microchannel geometries. Cells rarely swim in the central part of the channel cross-section, instead traveling along the intersection of the channel walls ("channel corners"). When the channel turns sharply, cells leave the corner, continuing ahead until hitting the opposite wall of the channel, with a distribution of departure angles, the latter being modulated by fluid viscosity. If the channel bend is smooth, cells depart from the inner wall when the curvature radius is less than a threshold value close to 150 μm. Specific wall shapes are able to preferentially direct motile cells. As a consequence of swimming along the corners, the domain occupied by cells becomes essentially one-dimensional, leading to frequent collisions, and needs to be accounted for when modeling the behavior of populations of migratory cells and considering how sperm populate and navigate the female tract. The combined effect of viscosity and three-dimensional architecture should be accounted for in future in vitro studies of sperm chemoattraction.cell swimming | motility | reproduction | thigmotaxis S perm motility is influenced by surfaces; this is most simply and strikingly evident in the accumulation of cells on the surfaces of microscope slides and coverslips, a phenomenon known to every andrologist. The effect and its causes have been investigated extensively through a variety of approaches, including microscopy (1-4), computational fluid mechanics, (5-9), molecular dynamics (10), and mathematical analysis (11). Principal points addressed by previous studies are the extent to which surface accumulation is a generic feature fluid dynamic effect associated with near-wall swimming, the role of specialized flagellar beat patterns, species-specific morphology, and the relative prevalence of swimming "near" as opposed to "against" walls; discussion of these questions can be found in recent editorials (12, 13). There has also been a resurgence of interest recently in the fluid mechanics of motile bacteria (14-17) and generic models for swimming cells (11,(18)(19)(20).Previous studies have usually focused on the behavior of a cell near a single planar surface or between a pair of planar surfaces, modeling the interior of a haemocytometer or similar device; however, both the female reproductive tract and microfluidic in vitro fertilization (IVF) devices present sperm with a much more confined and potentially tortuous geometry. The fallopian tubes consist of ciliated epithelium (21), the distance between opposed epithelial surfaces bein...
Experimental results on mean inclination angle and its fluctuation due to thermal noise in tank-treading motion of a vesicle in shear flow as a function of vesicle excess area, normalized shear rate, viscosity, and viscosity contrast between inner and outer fluids, , are presented. Good quantitative agreement with theory made for was found. At the dependence is altered significantly. Dependence of the vesicle shape on shear rate is consistent with theory. A tank-treading velocity of the vesicle membrane is found to be a periodic function close to that predicted by theory.
Semiflexible polymers subject to hydrodynamic forcing play an important role in cytoskeletal motions in the cell, particularly when filaments guide molecular motors whose motions create flows. Near hyperbolic stagnation points, filaments experience a competition between bending elasticity and tension and are predicted to display suppressed thermal fluctuations in the extensional regime and a buckling instability under compression. Using a microfluidic cross-flow geometry, we verify these predictions in detail, including a fluctuation-rounded stretch-coil transition of actin filaments.
We report the first experimental phase diagram of vesicle dynamical states in a shear flow presented in a space of two dimensionless parameters suggested recently by V. Lebedev et al. To reduce errors in the control parameters, 3D geometrical reconstruction and determination of the viscosity contrast of a vesicle in situ in a plane Couette flow device prior to the experiment are developed. Our results are in accord with the theory predicting three distinctly separating regions of vesicle dynamical states in the plane of just two self-similar parameters.
An approach to quantitatively study vesicle dynamics as well as biologically-related micro-objects in a fluid flow, which is based on the combination of a dynamical trap and a control parameter, the ratio of the vorticity to the strain rate, is suggested. The flow is continuously varied between rotational, shearing, and elongational in a microfluidic 4-roll mill device, the dynamical trap, that allows scanning of the entire phase diagram of motions, i.e., tank-treading (TT), tumbling (TU), and trembling (TR), using a single vesicle even at ؍ in/out ؍ 1, where in and out are the viscosities of the inner and outer fluids. This cannot be achieved in pure shear flow, where the transition between TT and either TU or TR is attained only at >1. As a result, it is found that the vesicle dynamical states in a general are presented by the phase diagram in a space of only 2 dimensionless control parameters. The findings are in semiquantitative accord with the recent theory made for a quasi-spherical vesicle, although vesicles with large deviations from spherical shape were studied experimentally. The physics of TR is also uncovered. U nderstanding the rheology of biofluids remains a great challenge, whose progress relies, in a large part, on detailed studies of the dynamics of a single cell. Vesicles are a model system used to study the dynamic behavior of biological cells, similar in some respects to red blood cells, and their dynamics in shear flow have been the subject of intensive theoretical (1-8), numerical (9-13), and experimental (14-18) investigations.A vesicle is a droplet of viscous fluid encapsulated by a phospholipid bilayer membrane suspended in a fluid of either the same or different viscosity as the inner one. Both the volume and the surface area of the vesicle are conserved. The former means that the vesicle membrane is considered to be impermeable, at least on the time scale of the experiment, and the latter means that the membrane dilatation is neglected since it is 2D fluid (1,2). Experimental, theoretical, and computational efforts during the last decade led to the observation and characterization of 3 states in vesicle dynamics in shear flow. The existence of the first 2, tank-treading (TT) and tumbling (TU), and the transition between them were already predicted by a phenomenological model of Keller and Skalak (19) and its further extensions (2,11,12). Two control parameters, the excess area ⌬ ϭ A/R 2 -4 and the viscosity contrast ϭ in / out , determine the transition line c (⌬) between TT and TU, which is independent of the shear rate ␥ in the approximation of a fixed vesicle shape, with the vesicle inclination angle with respect to the flow direction as the only dynamical variable (2,9,10,16-19). Here, R is the effective vesicle radius, related to the volume via V ϭ 4/3R 3 , A is the vesicle surface area, and in and out are the viscosities of the inner and outer fluids. Another analytical approach based on a quasi-spherical vesicle approximated by a spherical harmonics expansion used a perturb...
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