Session M6: Biofluids: Microswimmers III

The curved shape of the bacterium \textit{Caulobacter crescentus} enhances colonization of surfaces in flow

Bacteria thrive in all types of fluid environments; flow is thus a ubiquitous aspect of their lives. Bacteria have evolved a variety of cellular components contributing to their growth in specific environments. However, cellular features that help them survive and develop in flow have been rarely characterized. Here, we show that \textit{Caulobacter crescentus} may have evolved its curved shape to enhance the colonization of surfaces in flow. \textit{C. crescentus} curvature is preserved in the wild but straight mutants have no known growth disadvantage in standard laboratory conditions. Leveraging microfluidics and single-cell imaging, we demonstrate that curvature enhances surface colonization in flow, promoting the formation of larger microcolonies. Cells attach to a surface from a single pole, so that flow affects their orientation. In flow, viscous forces generate a torque on the curved cell body, which reorients the cell in the direction of the flow. The curved cell appears to arc above the surface, optimally orienting its unattached pole towards the surface. This reduces the distance between the surface and the pole, thereby enhancing attachment of its progeny. Additionally, we show that curved shape enhances colony spreading across the direction of the flow, generating more robust biofilm compared to straight mutants.   

Chemotactic decision making in swimming microorganisms

Swimming cells are often guided by chemical gradients (``chemotaxis'') to search for nutrients, hosts, and mates, and to avoid predators and noxious substances. It remains unclear, however, how variable the chemotactic abilities of cells are among cells of one species, and whether there are better ``decision makers'' within a population. Inspired by studies in macro-organism ecology, we fabricated a microfluidic ``T-maze'' in which marine bacteria are subjected to a chemical attractant gradient at each of a series of consecutive T-junctions. We used video microscopy to capture the motion of thousands of bacteria as they migrate up or down the gradient at each subsequent junction. This approach provides detailed statistics at both the single-cell and population levels, while simultaneously sorting the cells by chemotactic ability. Using a range of bacteria, we demonstrate how the microfluidic T-maze allows us to sort the better decision-making cells in the population, opening the door for improved efficiency of a range of microbial processes in nature and industry.   

The deadly swimming of Cercariae: an unusual Stokesian swimmer

Schistosomiasis, also known as Bilharzia, is a Neglected Tropical Disease (NTD) caused by a parasitic Trematode blood fluke worm. In terms of socio-economic and public health impact, Schistosomiasis is second only to Malaria as the most devastating parasitic disease in tropical countries; with roughly 200 million people infected at any time world-wide and up to 200,000 deaths every year. The infectious form of the parasite, known as Cercariae, emerge from snails into freshwater and infect humans by directly burrowing into the skin. Thus, anyone in contact with infected waters is at risk, which mostly includes children. By establishing a safe experimental means of studying the Cercariae in our lab, we report here their unusual swimming dynamics which include both head-first and tail-first swimming modes. These swimming modes are crucial for the chemotactic activity of Cercariae which allows them to seek out and burrow into human skin. By experimental and analytical means, we demonstrate that Cercariae break symmetry and achieve locomotion at small Reynolds number differently when compared to well-known methods involving traveling waves in the flagellum or chiral beating. Although they utilize the well-known drag anisotropy of a slender body in Stokes flow, the geometry and kinematics of their propulsion mechanism is novel. Based on these results, we propose a new kind of simple Stokesian swimmer (T-joint swimmer) in an attempt to explain the evolutionary advantages of this novel swimming mechanism. Using the above physical insights from a biological and global-health standpoint, we explore ways to hinder the chemotactic capabilities of this parasite.   

Shape and shear guide sperm cells spiraling upstream

A major puzzle in biology is how mammalian sperm determine and maintain the correct swimming direction during the various phases of the sexual reproduction process. Currently debated mechanisms for sperm long range travel vary from peristaltic pumping to temperature sensing (thermotaxis) and direct response to fluid flow (rheotaxis), but little is known quantitatively about their relative importance. Here, we report the first quantitative experimental study of mammalian sperm rheotaxis. Using microfluidic devices, we investigate systematically the swimming behavior of human and bull sperm over a wide 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 a stable upstream spiraling motion of sperm cells, thus providing a generic and robust rectification mechanism to support mammalian fertilization. To rationalize these findings, we identify a minimal mathematical model that is capable of describing quantitatively the experimental observations.   

The unique low-Reynolds-number spinning hydrodynamics of release of a giant multinucleate multiflagellate zoospore

Asexual reproduction in aquatic algal species of Vaucheria occurs by the formation of large multinucleate zoospores formed within elongated club-shaped zoosporangia at the tips of young branches. During development, the zoosporangia are separated from the rest of the thallus by membranes, resulting in multiple chambers hosting zoospores which will be released and dispersed in the surrounding aqueous environment. The apical gelatinization of the zoosporangial tip, together with the turgor pressure in the segregated portion of the filament, lead to a narrow aperture through which the zoospore escapes. However ordinary this may seem, Vaucheria zoospores have a unique multiflagellated patterned surface that warrants helicoidal flow entrainment at relatively high speeds, and which enables them to undergo a spinning motion that elastohydrodynamically assists the rather unfavorable escape maneuver. Experimental observations of this phenomenon, together with quantitative interpretations, are provided in this talk.   

Random walk of microswimmers: puller and pusher cases

Swimming at a micrometer scale demands particular strategies. Indeed when inertia is negligible as compared to viscous forces (i.e. Reynolds number Re is lower than unity), hydrodynamics equations are reversible in time. To achieve propulsion a low Reynolds number, swimmers must then deform in a way that is not invariant under time reversal. Here we investigate the dispersal properties of self propelled organisms by means of microscopy and cell tracking. Our systems of interest are, on the one hand, the microalga Chlamydomonas Reinhardtii, a puller-type swimmer and on the other hand, Lingulodinium polyedrum, a pusher. Both are quasi-spherical single celled alga. In the case of dilute suspensions, we show that tracked trajectories are well modelled by a correlated random walk. This process is based on short time correlations in the direction of movement called persistence. At longer times, correlations are lost and a standard random walk characterizes the trajectories. Finally we show how drag forces modify the characteristics of this particular random walk.   

How to be invisible as a microscopic swimmer

Microscopic plankton live a difficult life in open waters, having to continuously scan large amounts of water for food and mates, and hide from predators at the same time. In the absence of vision at these small scales, all interactions are dominated by chemical and hydromechanical cues. Thus, there is an evolutionary pressure to minimize the hydromechanical disturbance generated during processes such as feeding and locomotion. We report experimental observations that breast stroke swimming plankton generate a fluid disturbance that decays faster with distance than what is predicted from the commonly used stresslet model of a self-propelled organism. We rationalize these observations by using a three-Stokeslet model of a breast stroke swimmer, and show that it is possible for a swimmer to dramatically reduce its fluid disturbance by appropriately positioning the propulsive apparatus. A generalization of this concept may be used in understanding the large diversity of shapes and swimming modes found in the plankton world.   

Viscous constraints on predator:food size ratios in microscale feeding

Small organisms such as protists or copepods may try to capture food by manipulating food with cilia, limbs, or feeding appendages. At these small scales, viscous flow may complicate the ability of a feeding appendage to closely approach a food particle. As a simplified but tractable model of such feeding approach, we consider the problem of two spheres approaching in a Stokes fluid. The first ``feeding'' sphere, which represents a body part or feeding appendage, is pushed with a constant force towards a force-free ``food'' sphere. When the feeding sphere reaches within a cutoff distance of the food sphere we assume that nonhydrodynamic interactions lead to capture. We examine approach for a range of size ratios between the feeding and food sphere. To investigate the approach efficiency, we examine the time required for the feeding sphere to capture the food sphere, as well as how far the feeding sphere must move before it captures the food sphere. We also examine the effect of varying the cutoff distance for capture. We find that hydrodynamic interactions strongly affect the results when the size of the spheres is comparable. We describe what relative sizes between feeding sphere and food particles may be most effective for food capture.   

Mass transfer effect of the stalk contraction-relaxation cycle of \textit{Vorticella convallaria}

\textit{Vorticella convallaria} is a genus of protozoa living in freshwater. Its stalk contracts and coil pulling the cell body towards the substrate at a remarkable speed, and then relaxes to its extended state much more slowly than the contraction. However, the reason for \textit{Vorticella}'s stalk contraction is still unknown. It is presumed that water flow induced by the stalk contraction-relaxation cycle may augment mass transfer near the substrate. We investigated this hypothesis using an experimental model with particle tracking velocimetry and a computational fluid dynamics model. In both approaches, \textit{Vorticella} was modeled as a solid sphere translating perpendicular to a solid surface in water. After having been validated by the experimental model and verified by grid convergence index test, the computational model simulated water flow during the cycle based on the measured time course of stalk length changes of \textit{Vorticella}. Based on the simulated flow field, we calculated trajectories of particles near the model \textit{Vorticella}, and then evaluated the mass transfer effect of \textit{Vorticella}'s stalk contraction based on the particles' motion.   

Direct measurement of the forces generated by an undulatory microswimmer

\textit{C. elegans} is a millimeter-sized nematode which has served as a model organism in biology for several decades, primarily due to its simple anatomy. Employing an undulatory form of locomotion, this worm is capable of propelling itself through various media. Using a micropipette deflection technique, in conjunction with high speed imaging, we directly measure the time-varying forces generated by \textit{C. elegans}. We observe excellent agreement between our measured forces and the predictions of resistive force theory, through which we determine the drag coefficients of the worm. We also perform the direct force measurements at controlled distances from a single solid boundary as well as between two solid boundaries. We extract the drag coefficients of the worm to quantify the influence of the boundary on the swimming and the hydrodynamic forces involved.