Efficiency optimization and symmetry-breaking in a model of ciliary locomotion

A variety of swimming microorganisms, called ciliates, exploit the bending of a large number of small and densely-packed organelles, termed cilia, in order to propel themselves in a viscous fluid. We consider a spherical envelope model for such ciliary locomotion where the dynamics of the individual cilia are replaced by that of a continuous overlaying surface allowed to deform tangentially to itself. Employing a variational approach, we determine numerically the time-periodic deformation of such surface which leads to low-Reynolds locomotion with minimum rate of energy dissipation (maximum efficiency). Employing both Lagrangian and Eulerian points of views, we show that in the optimal swimming stroke, individual cilia display weak asymmetric beating, but that a significant symmetry-breaking occurs at the organism level, with the whole surface deforming in a wave-like fashion reminiscent of metachronal waves of biological cilia. This wave motion is analyzed using a formal modal decomposition, is found to occur in the same direction as the swimming direction, and is interpreted as due to a spatial distribution of phase-differences in the kinematics of individual cilia. Using additional constrained optimizations, as well as a constructed analytical ansatz, we derive a complete optimization diagram where all swimming efficiencies, swimming speeds, and amplitude of surface deformation can be reached, with the mathematically optimal swimmer, of efficiency one half, being a singular limit. Biologically, our work suggests therefore that metachronal waves may allow cilia to propel cells forward while reducing the energy dissipated in the surrounding fluid.Comment: 29 pages, 20 figure

Shape of optimal active flagella

Many eukaryotic cells use the active waving motion of flexible flagella to self-propel in viscous fluids. However, the criteria governing the selection of particular flagellar waveforms among all possible shapes has proved elusive so far. To address this question, we derive computationally the optimal shape of an internally-forced periodic planar flagellum deforming as a travelling wave. The optimum is here defined as the shape leading to a given swimming speed with minimum energetic cost. To calculate the energetic cost though, we consider the irreversible internal power expanded by the molecular motors forcing the flagellum, only a portion of which ending up dissipated in the fluid. This optimisation approach allows us to derive a family of shapes depending on a single dimensionless number quantifying the relative importance of elastic to viscous effects: the Sperm number. The computed optimal shapes are found to agree with the waveforms observed on spermatozoon of marine organisms, thus suggesting that these eukaryotic flagella might have evolved to be mechanically optimal.Comment: 10 pages, 5 figure

Unsteady feeding and optimal strokes of model ciliates

The flow field created by swimming microorganisms not only enables their locomotion but also leads to advective transport of nutrients. In this paper we address analytically and computationally the link between unsteady feeding and unsteady swimming on a model microorganism, the spherical squirmer, actuating the fluid in a time-periodic manner. We start by performing asymptotic calculations at low P\'eclet number (Pe) on the advection-diffusion problem for the nutrients. We show that the mean rate of feeding as well as its fluctuations in time depend only on the swimming modes of the squirmer up to order Pe^(3/2), even when no swimming occurs on average, while the influence of non-swimming modes comes in only at order Pe^2. We also show that generically we expect a phase delay between feeding and swimming of 1/8th of a period. Numerical computations for illustrative strokes at finite Pe confirm quantitatively our analytical results linking swimming and feeding. We finally derive, and use, an adjoint-based optimization algorithm to determine the optimal unsteady strokes maximizing feeding rate for a fixed energy budget. The overall optimal feeder is always the optimal steady swimmer. Within the set of time-periodic strokes, the optimal feeding strokes are found to be equivalent to those optimizing periodic swimming for all values of the P\'eclet number, and correspond to a regularization of the overall steady optimal.Comment: 26 pages, 11 figures, to appear in Journal of Fluid Mechanic

Optimal feeding is optimal swimming for all P\'eclet numbers

Cells swimming in viscous fluids create flow fields which influence the transport of relevant nutrients, and therefore their feeding rate. We propose a modeling approach to the problem of optimal feeding at zero Reynolds number. We consider a simplified spherical swimmer deforming its shape tangentially in a steady fashion (so-called squirmer). Assuming that the nutrient is a passive scalar obeying an advection-diffusion equation, the optimal use of flow fields by the swimmer for feeding is determined by maximizing the diffusive flux at the organism surface for a fixed rate of energy dissipation in the fluid. The results are obtained through the use of an adjoint-based numerical optimization implemented by a Legendre polynomial spectral method. We show that, to within a negligible amount, the optimal feeding mechanism consists in putting all the energy expended by surface distortion into swimming - so-called treadmill motion - which is also the solution maximizing the swimming efficiency. Surprisingly, although the rate of feeding depends strongly on the value of the P\'eclet number, the optimal feeding stroke is shown to be essentially independent of it, which is confirmed by asymptotic analysis. Within the context of steady actuation, optimal feeding is therefore found to be equivalent to optimal swimming for all P\'eclet numbers.Comment: 14 pages, 6 figures, to appear in Physics of Fluid

Using Surface-Motions for Locomotion of Microscopic Robots in Viscous Fluids

Microscopic robots could perform tasks with high spatial precision, such as acting in biological tissues on the scale of individual cells, provided they can reach precise locations. This paper evaluates the feasibility of in vivo locomotion for micron-size robots. Two appealing methods rely only on surface motions: steady tangential motion and small amplitude oscillations. These methods contrast with common microorganism propulsion based on flagella or cilia, which are more likely to damage nearby cells if used by robots made of stiff materials. The power potentially available to robots in tissue supports speeds ranging from one to hundreds of microns per second, over the range of viscosities found in biological tissue. We discuss design trade-offs among propulsion method, speed, power, shear forces and robot shape, and relate those choices to robot task requirements. This study shows that realizing such locomotion requires substantial improvements in fabrication capabilities and material properties over current technology.Comment: 14 figures and two Quicktime animations of the locomotion methods described in the paper, each showing one period of the motion over a time of 0.5 milliseconds; version 2 has minor clarifications and corrected typo

Mixing and transport by ciliary carpets: a numerical study

We use a 3D computational model to study the fluid transport and mixing due to the beating of an infinite array of cilia. In accord with recent experiments, we observe two distinct regions: a fluid transport region above the cilia and a fluid mixing region below the cilia tip. The metachronal wave due to phase differences between neighboring cilia is known to enhance the fluid transport above the ciliary tip. In this work, we show that the metachronal wave also enhances the mixing rates in the sub-ciliary region, often simultaneously with the flow rate enhancement. Our results suggest that this simultaneous enhancement in transport and mixing is due to an enhancement in shear flow. As the flow above the cilia increases, shear rate in the fluid increases and such shear enhances stretching, which is an essential ingredient for mixing. Estimates of the mixing time scale indicate that, compared to diffusion, the mixing due to the cilia beat may be significant and sometimes dominates chemical diffusion.Comment: submitted to Journal of Fluid Mechanic