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Near-wall rheotaxis of the ciliate Tetrahymena induced by the kinesthetic sensing of cilia - PubMed

  • ️Fri Jan 01 2021

Near-wall rheotaxis of the ciliate Tetrahymena induced by the kinesthetic sensing of cilia

Takuya Ohmura et al. Sci Adv. 2021.

Abstract

To survive in harsh environments, single-celled microorganisms autonomously respond to external stimuli, such as light, heat, and flow. Here, we elucidate the flow response of Tetrahymena, a well-known single-celled freshwater microorganism. Tetrahymena moves upstream against an external flow via a behavior called rheotaxis. While micrometer-sized particles are swept away downstream in a viscous flow, what dynamics underlie the rheotaxis of the ciliate? Our experiments reveal that Tetrahymena slides along walls during upstream movement, which indicates that the cells receive rotational torque from shear flow to control cell orientation. To evaluate the effects of the shear torque and propelling speed, we perform a numerical simulation with a hydrodynamic model swimmer adopting cilia dynamics in a shear flow. The swimmer orientations converge to an upstream alignment, and the swimmer slides upstream along a boundary wall. The results suggest that Tetrahymena automatically responds to shear flow by performing rheotaxis using cilia-stalling mechanics.

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Figures

Fig. 1.
Fig. 1.. Motility and orientation of T. pyriformis under shear flow.

(A) Experimental setup for the observation of cells in a rectangular microfluidic channel. We observed cells on the xy bottom wall of the channel by microscopy. The cells experienced shear flow, which was assumed to involve linear shear close to the bottom wall. (B) A typical trajectory of a rheotaxic cell. The cell slid against the flow on the bottom wall. The top blue vector represents the flow direction. The black vectors represent the moving directions of the cell. The time interval of each position is 30 ms. Scale bar, 200 μm. The inset figure presents a schematic picture of the measured parameters. (C) Plot of the x velocity vx as a function of the shear rate. Plots in the red area represent positive rheotaxis. When the shear rate was higher than a characteristic rheotaxic shear rate 19.4 s−1 (gray area), the cells showed negative rheotaxis or were swept away downstream. (D) Plot of the y velocity vy as a function of the shear rate. (E) Plot of the speed as a function of the shear rate. (F) 3D histogram of θxy, the angle of the long axis on an ellipse-fitted cell. With increasing shear rate, θxy converged. (G) Plot of θxy as a function of the shear rate. (H) 2D nematic-order parameter between θxy and the flow direction. The value quickly increased around the characteristic rheotaxic shear rate. Error bars represent the SD.

Fig. 2.
Fig. 2.. Asymmetric ciliary beatings around a sliding cell under shear flow.

(A) Experimental setup for fluorescent observation with light sheet microscopy. Cells were placed in a fluorinated ethylene polypropylene (FEP) tube and allowed to flow. (B) A schematic figure of the cells inside the tube (side view). In the tube, the cells experienced a Hagen-Poiseuille flow and slid upstream adjacent to the inner wall. (C) A schematic figure of the cells inside the tube (front view). The light sheet was aligned along the tube, and the sliding cells were scanned through the FEP tube. (D) Snapshots of ciliary beating around a sliding cell. Left: The sliding cell on the bottom wall. Scale bar, 40 μm. We traced the cilia in the pictures using pink lines. Top: Cilia that were not attached to the wall were actively beating and when the cell swam in bulk water. Bottom: The attached cilia were inactive. Snapshots were taken at 5-ms intervals. Scale bar, 10 μm.

Fig. 3.
Fig. 3.. Model of ciliates swimming in a shear flow close to a nonslip boundary.

(A) A 3D numerical swimmer of a mathematical model of ciliates is defined as a rigid ellipsoid (a gray object). Its surface is discretized into triangular elements for the boundary element method. Each node in an element has a thrust point force slightly far from the rigid surface (blue vectors). (B) A 3D schematic of the numerical system. The swimmer is located in a linear shear flow close to a nonslip wall. Black vectors represent the shear flow. (C) Parameter setup. An ellipsoid represents a swimmer, and the black vectors show the swimming direction. Top: A schematic on the xz plane, where θxz is the angle between the longitudinal axis of the swimmer and the wall. Bottom: A schematic on the xy plane, where θxy is the angle between the longitudinal axis and the flow direction.

Fig. 4.
Fig. 4.. Spherical and ellipsoidal swimmers with and without SBA in a shear flow.

(A to D) Snapshots of trajectories in the xz plane of numerical swimmers under shear flow under four conditions. The color depth of objects in the plots becomes darker over time (from pale blue to deep blue). The flow direction points to the right. The shear rate γ*·=0.5, the initial angle θi = 60.0°, and the initial position (x, y, z) = (0,0,0) are the same in all cases. (A and B) A spherical swimmer and an ellipsoidal swimmer without the SBA. Both swimmers attached to the wall once, but they could not stay on the wall. (C) A spherical swimmer with the SBA. The swimmer stayed on the wall for a few moments but was eventually swept away. (D) An ellipsoidal swimmer with the SBA. After attaching to a wall, the swimmer started sliding in the direction opposite to the flow. (E) Trajectories of the four swimmers in (A) to (D). The black vectors indicate the directions of the trajectories. Only the ellipsoidal swimmer with the SBA made upstream progress. (F) Time evolutions of θxz. All swimmers started with motion in the bottom-right direction. The spherical and ellipsoidal swimmers without the SBA (dark red and dark blue) continuously rotated, which indicates that they were swept by the shear flow. A step in the simulation represents 0.0881 s in real time. The spherical swimmer with the SBA (light red) gradually changed its θxz until 4000 steps (= 3.53 s) and then started rotating. In the case of the ellipsoidal swimmer with the SBA, θxz converged to 171.1°.

Fig. 5.
Fig. 5.. Evaluation of rheotaxis of numerical swimmers.

(A) Dependence of the initial xy angle θi. Top: Trajectories on the xz plane. None of the swimmers detached from the wall. Bottom: Trajectories on the xy plane. In all cases, the swimmers lastly slid against a flow parallel to the x axis. (B) Time evolutions of the xy angle. In all cases, θxy converged to 180°. The color depth in the plots denotes the change in θi. In all cases, γ*·=0.5 and the initial θxz = 60.0° were fixed. (C) The x velocities of the swimmers with the shear rate. The x velocity of the ellipsoidal swimmers with the SBA linearly decreased until γ·=17.0 s−1 (filled red triangles). Above γ·c=19.8 s−1, the ellipsoidal swimmers were swept in the flow; therefore, the velocities were large and positive (empty red triangles). The spherical swimmer stayed on the wall until γ·=5.1 s−1 (filled blue triangles) and detached at γ·=5.7 s−1 (empty blue triangles). The gray area in the plot represents the shear rate at which the ellipsoidal swimmer was swept downstream including the case with sustaining the slide motion as defined in the experiments.

Fig. 6.
Fig. 6.. Schematic figures of the dynamics of rheotaxis and alignment.

(A) The green and blue ellipsoids represent the swimmer, and the light gray area represents the SBA. Tb is the torque arising from the asymmetricity of the thrust force. Ts is the combined torque from a shear flow and the hydrodynamic interaction with a wall. As shown in the top-right and bottom-right figures, the swimmer detached at Tb < Ts, and the swimmer could stay on the wall at Tb > Ts. (B) The swimmer’s orientation θxy automatically becomes aligned with the flow direction when the swimmer slides along a wall due to a coupling of the shear torque and self-propelled torque.

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