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.
The eukaryotic flagellum beats periodically, driven by the oscillatory dynamics of molecular motors, to propel cells and pump fluids. Small, but perceivable fluctuations in the beat of individual flagella have physiological implications for synchronization in collections of flagella as well as for hydrodynamic interactions between flagellated swimmers. Here, we characterize phase and amplitude fluctuations of flagellar bending waves using shape mode analysis and limit cycle reconstruction. We report a quality factor of flagellar oscillations, $Q=38.0\pm 16.7$ (mean$\pm$s.e.). Our analysis show…
Eukaryotic flagella are active structures with a complex architecture of microtubules, motor proteins and elastic links. They are capable of whiplike motions driven by motors sliding along filaments that are themselves constrained at an end. Here, we show that active, self-propelled particles that are connected together to form a single chain that is anchored at one end can produce the graceful beating motions of flagella. We use a combination of numerical simulations, scaling analysis and mean field continuum elastic theory to demarcate the phase diagram for this type of oscillatory motion as…
Confinement and wall effects are known to affect the kinematics and propulsive characteristics of swimming microorganisms. When a solid body is dragged through a viscous fluid at constant velocity, the presence of a wall increases fluid drag, and thus the net force required to maintain speed has to increase. In contrast, recent optical trapping experiments have revealed that the propulsive force generated by human spermatozoa is decreased by the presence of boundaries. Here, we use a series of simple models to analytically elucidate the propulsive effects of a solid boundary on passively actua…
Living creatures exhibit a remarkable diversity of locomotion mechanisms, evolving structures specialised for interacting with their environment. In the vast majority of cases, locomotor behaviours such as flying, crawling, and running, are orchestrated by nervous systems. Surprisingly, microorganisms can enact analogous movement gaits for swimming using multiple, fast-moving cellular protrusions called cilia and flagella. Here, I demonstrate intermittency, reversible rhythmogenesis, and gait mechanosensitivity in algal flagella, to reveal the active nature of locomotor patterning. In addition…
Organelle size control is a fundamental question in biology that demonstrates the fascinating ability of cells to maintain homeostasis within their highly variable environments. Theoretical models describing cellular dynamics have the potential to help elucidate the principles underlying size control. Here, we perform a detailed study of the active disassembly model proposed in [Fai et al, Length regulation of multiple flagella that self-assemble from a shared pool of components, eLife, 8, (2019): e42599]. We construct a hybrid system which is shown to be well-behaved throughout the domain. We…
Flagellar motility is critical to natural and many forms of assisted reproduction. Rhythmic beating and wave propagation by the flagellum propels sperm through fluid and enables modulation between penetrative progressive motion, activated side-to-side yaw and hyperactivated motility associated with detachment from epithelial binding. These motility changes occur in response to the properties of the surrounding fluid environment, biochemical activation state, and physiological ligands, however a parsimonious mechanistic explanation of flagellar beat generation that can explain motility modulati…
Self-propelled point-like particles move along circular trajectories when their translocation velocity is constant and the angular velocity related to their orientation vector is also constant. We investigate the collective behavior of ensembles of such circle swimmers by Brownian dynamics simulations. If the particles interact via a "velocity-trajectory coordination" rule within neighboring particles, a self-organized vortex pattern emerges. This vortex pattern is characterized by its particle-density correlation function $G_ρ$, the density correlation function $G_c$ of trajectory centers, an…
Motile eukaryotic cells propel themselves in viscous fluids by passing waves of bending deformation down their flagella. An infinitely long flagellum achieves a hydrodynamically optimal low-Reynolds number locomotion when the angle between its local tangent and the swimming direction remains constant along its length. Optimal flagella therefore adopt the shape of a helix in three dimensions (smooth) and that of a sawtooth in two dimensions (non-smooth). Physically, biological organisms (or engineered micro-swimmers) must expend internal energy in order to produce the waves of deformation respo…
The motility of cilia and flagella is driven by thousands of dynein motors that hydrolyze adenosine triphosphate (ATP). Despite decades of genetic, biochemical, structural and biophysical studies, some aspects of ciliary motility remain elusive, such as the regulation of beating patterns and the energetic efficiency of these nanomachines. Here, we introduce an experimental method to measure ATP consumption of actively beating axonemes on a single-cell level. We encapsulated individual sea urchin sperm with demembranated flagellum inside water-in-oil emulsion droplets and measured the axonemes …
Cilia and flagella are actively bending slender organelles, performing functions such as motility, feeding and embryonic symmetry breaking. We review the mechanics of viscous-dominated microscale flow, including time-reversal symmetry, drag anisotropy of slender bodies, and wall effects. We focus on the fundamental force singularity, higher order multipoles, and the method of images, providing physical insight and forming a basis for computational approaches. Two biological problems are then considered in more detail: (1) left-right symmetry breaking flow in the node, a microscopic structure i…
Cilia and flagella are hairlike organelles that propel cells through fluid. The active motion of the axoneme, the motile structure inside cilia and flagella, is powered by molecular motors of the dynein family. These motors generate forces and torques that slide and bend the microtubule doublets within the axoneme. To create regular waveforms the activities of the dyneins must be coordinated. It is thought that coordination is mediated by stresses due to radial, transverse, or sliding deformations, that build up within the moving axoneme. However, which particular component of the stress regul…
Motivated by recent advances in vesicle engineering, we consider theoretically the locomotion of shape-changing bilayer vesicles at low Reynolds number. By modulating their volume and membrane composition, the vesicles can be made to change shape quasi-statically in thermal equilibrium. When the control parameters are tuned appropriately to yield periodic shape changes which are not time-reversible, the result is a net swimming motion over one cycle of shape deformation. For two classical vesicle models (spontaneous curvature and bilayer coupling), we determine numerically the sequence of vesi…
Recent experiments proposed to use confined bacteria in order to generate flows near surfaces. We develop a mathematical and a computational model of this fluid transport using a linear superposition of fundamental flow singularities. The rotation of a helical bacterial flagellum induces both a force and a torque on the surrounding fluid, both of which lead to a net flow along the surface. The combined flow is in general directed at an angle to the axis of the flagellar filament. The optimal pumping is thus achieved when bacteria are tilted with respect to the direction in which one wants to m…
Peritrichous bacteria swim in viscous fluids by rotating multiple helical flagellar filaments. As the bacterium swims forward, all its flagella rotate in synchrony behind the cell in a helical bundle. When the bacterium changes its direction, the flagellar filaments unbundle and reorient the cell for a short period of time before returning to their bundled state and resuming swimming. This rapid bundling and unbundling is, at its heart, a mechanical process whereby hydrodynamic interactions balance with elasticity to determine the time-varying deformation of the filaments. Inspired by this bio…
Spatially localised defect structures emerge spontaneously in a hydrodynamic description of an active polar fluid comprising polar 'actin' filaments and 'myosin' motor proteins that (un)bind to filaments and exert active contractile stresses. These emergent defect structures are characterized by distinct textures and can be either static or mobile - we derive effective equations of motion for these 'extended particles' and analyse their shape, kinetics, interactions and scattering. Depending on the impact parameter and propulsion speed, these active defects undergo elastic scattering or merger…
Active forces occurring within cells can drive crucial biological processes that involve spontaneous organization and shape change, such as cell division. Motivated by recent in vitro experiments of nematic droplets of cytoskeletal filaments and motors that self-organize and divide, we present a minimal hydrodynamic model that combines the nonequilibrium kinetics of motor-filament interactions with equilibrium nematic phase separation. The motors organize within droplets and structure filaments into polarized aster defects. At large motor activity, they can even deform or divide the droplet, o…
During the early-stages of embryo development, morphogenesis--- the emergence of shape and form in living organisms--- is almost exclusively associated with monolayers of tightly bound epithelial cells. To understand how such tissues change their shape, we construct a fully covariant active-hydrodynamic theory. At the cellular scale, stresses arise from apical contractility, mechanical response and the constraint of constant cell volume. Tissue-scale deformations emerge due to the balance between such cell-autonomous stresses and the displacement and shear of a low Reynolds number embedding fl…
Eukaryote cells have a flexible shape, which dynamically changes according to the function performed by the cell. One mechanism for deforming the cell membrane into the desired shape is through the expression of curved membrane proteins. Furthermore, these curved membrane proteins are often associated with the recruitment of the cytoskeleton, which then applies active forces that deform the membrane. This coupling between curvature and activity was previously explored theoretically in the linear limit of small deformations, and low dimensionality. Here we explore the unrestricted shapes of ves…
Active matter is characterized by its ability to induce motion by self-generated stress. In the case of a solid, such motion can lead to shape transformations. The stress-generating components can be anisotropic endowing the material with mesoscopic orientational order. It is currently unknown how the specific postions and orientations of these active constituents influence morphological changes. We study theoretically the effects of imposing topological point defects in the arrangements of the stress-generating components on the morphology of elastic active nematic shells. We show that topolo…
Biological cells can actively tune their intracellular architecture according to their overall shape. Here we explore the rheological implication of such coupling in a minimal model of a dense cellular material where each cell exerts an active mechanical stress along its axis of elongation. Increasing the active stress amplitude leads to several transitions. An initially hexagonal crystal motif is first destabilized into a solid with anisotropic cells. Increasing activity further, we find a re-entrant transition to a regime with finite hexatic order and finite shear modulus, in which cells arr…
Cells modify their volume in response to changes in osmotic pressure but it is usually assumed that other active shape variations do not involve significant volume fluctuations. Here we report experiments demonstrating that water transport in and out of the cell is needed for the formation of blebs, commonly observed protrusions in the plasma membrane driven by cortex contraction. We develop and simulate a model of fluid mediated membrane-cortex deformations and show that a permeable membrane is necessary for bleb formation which is otherwise impaired. Taken together our experimental and theor…
Active solids consume energy to allow for actuation, shape change, and wave propagation not possible in equilibrium. Whereas active interfaces have been realized across many experimental systems, control of three-dimensional (3D) bulk materials remains a challenge. Here, we develop continuum theory and microscopic simulations that describe a 3D soft solid whose boundary experiences active surface stresses. The competition between active boundary and elastic bulk yields a broad range of previously unexplored phenomena, which are demonstrations of so-called active elastocapillarity. In contrast …
