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Light moves artificial cilia to a complex beat

Cilia are microscopic hairs that grow on the outer surfaces of unicellular organisms, propelling the organisms through liquids by rhythmically beating in a specific pattern. This beating motion follows complex trajectories to achieve forward propulsion1, a feature known as non-reciprocal movement that it shares with human swimming techniques. But although this motion might be familiar, it is difficult to replicate using synthetic materials, because the beating is driven by the synchronized operation of many nanoscale molecular machines. Writing in Nature, Li et al.2 reveal that light-sensitive artificial molecular machines can be used to drive similarly complex motion in polymer cilia constructed from a single material.

Non-reciprocal motion is essential to movement in organisms that are micrometre-sized. A counterexample is the scallop, which is typically 10–20 centimetres long, and can swim forwards or backwards simply by opening and closing the two halves of its shell. This motion is reciprocal, because the opening and closing follow the same trajectories. By contrast, micrometre-sized unicellular organisms experience water as a viscous fluid, like a human swimming through honey, and so they cannot rely on inertia to push them forwards3. Therefore, to swim in water, such organisms have developed strategies involving complex non-reciprocal movement patterns. Some grow a long flagellum that rotates in a corkscrew-like way; others grow cilia; and still others have bodies that can take on spiral shapes4.

In artificial materials, cilium-like behaviour can be realized by inducing non-reciprocal shape transformations. Li and colleagues achieved this by using a molecular machine that flips back and forth in response to light5. These molecular machines can be bound covalently into a polymer made from a liquid-crystalline compound6. The approach is not entirely new; it has been used to mimic some of the complex movements found in the plant kingdom7 — from the winding of cucumber tendrils8 to the bursting of seedpods9, the snapping of flytraps10 and the light tracking of sunflowers11. But the authors have paired this technique with microfabrication, and with a model that predicts the motion of a cilium as a function of molecular misalignment with respect to its main axis, and the direction of illumination. The model can be used to guide the design of functional cilia.

Here, light plays a crucial part. When the polymer material absorbs light, a gradient of illumination intensity is established over the width of each cilium. As the light passes through the material, it activates the molecular machines, causing them to bend. This disrupts the liquid-crystalline order of the polymer and creates a gradient in molecular disorder12 (Fig. 1a). As a result, the homogeneous material is converted into two layers with different shape-shifting properties. The illuminated areas shrink preferentially along the orientation of the liquid-crystal molecules, which is also that of the molecular machines, whereas the ‘dark’ areas of the cilium remain unperturbed. This forces the cilium as a whole to both bend and twist.

figure 1

Figure 1 | Artificial hair-like structures (cilia) produce complex, collective beating patterns. a, Li et al.2 have designed cilia that exhibit beating dynamics, by incorporating light-sensitive molecular machines into a liquid-crystalline polymer material. When light shines through the material, it activates the molecular machines, which change shape and thereby deform the illuminated area, leaving the rest of the material unperturbed. b, The authors demonstrate that arrays of these cilia display collective motion through a shadowing effect: one cilium blocks the light aimed at its neighbour, but as soon as it starts beating, light shines on the neighbouring cilium, which, in turn, starts moving. This creates a domino effect through the array.

The authors found that they could establish feedback loops in this system. As the cilia twist, they expose different faces to the light, leading to changes in the travelling front of the light as it moves through each cilium. This change, in turn, affects the distribution between ordered and disordered areas over time, resulting in complex movements that Li et al. were able to manipulate by varying the intensity and direction of the illumination. And, once the light was switched off, the material relaxed by performing a movement that was different from the forward, light-induced movement. Li and co-workers concluded, therefore, that a on–off light cycle could induce a cilium beat that constitutes a non-reciprocal motion.

The authors then demonstrated that arrays of their beating cilia could exhibit collective motion by ‘communicating’ with each other through shadowing effects: when illumination induces one cilium to bend, it blocks the light aimed at its neighbour, and so on (Fig. 1b). This domino effect leads to the appearance of propagating waves, indicating that the movement of light-driven molecular machines can be transduced into collective movement. In this system, collective movement is induced by light, and could not be achieved by heat or chemical reactions.

The next frontier in this research could be to prepare the artificial cilia by going beyond microfabrication techniques and instead inducing the cilia to grow spontaneously through interactions between the constituent molecules13. Another challenge would be to engineer a way of avoiding the need for bespoke illumination conditions that involve continuously switching the light on and off14.

Although the authors showed that their artificial cilia could display complex movements reminiscent of cilia in living organisms, these structures are yet to rival their natural counterparts in terms of functionality. In biological systems, the beating of cilia is used to make a cell swim and to support the varied motile dynamics that enable the survival15 and competitive behaviour of bacteria16. Moving from motion to motility requires materials to show even better performance than that reported by Li and colleagues, calling for smaller structures, faster movement and higher amplitudes of oscillation. However, the authors’ work represents a crucial step towards functional artificial cilia. Along the way, it will doubtless inspire advances in microfluidics, and might even propel our understanding of cilia and cellular motility forward.

Nature 605, 37-38 (2022)

doi: https://doi.org/10.1038/d41586-022-01080-9

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Competing Interests

The authors declare no competing interests.

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