Simple mechanosense and response of cilia motion reveal the intrinsic habits of ciliates

Abstract

SignificanceSingle-celled microorganisms are important in ecosystems, and their behaviors impact the Earth’s environments. To survive in harsh environments, these organisms frequently act as though exercising discretion. How do they achieve such intelligent behaviors? In this work, we focused on the accumulation of ciliates on solid/fluid interfaces, where they can obtain sufficient nutrients and a stable environment. This phenomenon is not described in the standard hydrodynamics of microswimmers. Our experiment and simulation revealed that simple principles, the anisotropic shape of the cell and the mechanosensing nature of cilia, induce the accumulation of ciliates on solid/fluid interfaces. The contribution of our work is that a simple response of the cellular apparatus and fluid dynamics explain the apparently clever behavior of ciliates.

Influence of cellular shape on sliding behavior of ciliates

“…The map of the flow speeds visually supports this result (Figure 2(D). Similar results were also observed for T. pyriformis , and a small amount of flow was elicited by stopping ciliary beating, which was a key factor for swimmers to slide on the solid/fluid interface [7]. Therefore, it is suggested that the cilia of P. caudatum near the wall behave in the same manner as in the sliding motion of T. pyriformis , i.e., ciliary beating is stalled by attaching to the solid surface, which creates asymmetrical thrust forces around the cell, and consequently the cell experiences nose-down torque during the sliding motion on the solid surface.

10.1080/19420889.2018.1506666-F0001Figure 1.Sliding behavior of Paramecium caudatum on a glass surface.(A) A top view of P. caudatum sliding on a glass surface.

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“…One of the characteristic features of ciliates is the presence of cilia on the entire cell surface, whose beating motions induce thrust force to swim in water. Ciliates exhibit remarkable behaviors using cilia, such as helical swimming in bulk water [3–5] and accumulation on air/fluid and solid/fluid interfaces [6,7]. Since nutrition is deposited on the interfaces, it is advantageous that ciliates prefer the interfaces.…”

“…Recently, Ohmura et al . [7] revealed the mechanisms of the accumulating behavior of Tetrahymena pyriformis at a solid/fluid interface, which was induced by the sliding behavior of T. pyriformis on the surface. The experiments and numerical results exhibited a cellular shape and a mechanosensing feature of cilia, where a cilium contacting the wall almost stopped beating, causing the sliding behavior of T. pyriformis .…”

“…The glass plate had been coated with MPC, which prevented nonspecific interaction between the cell and the glass, as revealed in Ohmura et al . [7]. The transient dynamics from the bulk motion into sliding motion on the solid/fluid interface were directly yielded by side-view observation, where the cell was incident to the wall and slid after contacting the side wall (Figure 1(B)).…”

“…The traveling speed in bulk water was 948.9 ± 30.0 μms −1 (mean ± SEM, n = 73), and the traveling speed on the glass was 81.9 ± 3.4 μms −1 (mean ± SEM, n = 512), (Figure 2(B), which was qualitatively consistent with the simulation results of Ohmura et al . [7] where the sliding speeds were slower than the swimming speeds in bulk water. To examine whether the mechanisms of the sliding behavior of P. caudatum were the same as those of T. pyriformis , the flow fields generated by ciliary beating were determined by using 1.0 µm silica beads as tracer particles.…”