Highly Efficient Freestyle Magnetic Nanoswimmer

Letter pubs.acs.org/NanoLett

Highly Efficient Freestyle Magnetic Nanoswimmer Tianlong Li,†,‡,∥ Jinxing Li,†,∥ Konstantin I. Morozov,§ Zhiguang Wu,†,‡ Tailin Xu,† Isaac Rozen,† Alexander M. Leshansky,*,§ Longqiu Li,*,‡ and Joseph Wang*,† †

Department of Nanoengineering, University of California, San Diego, La Jolla, California 92093, United States State Key Laboratory of Robotics and System, Harbin Institute of Technology, Harbin, Heilongjiang 150001, China § Department of Chemical Engineering, TechnionIsrael Institute of Technology, Haifa 32000, Israel ‡

S Supporting Information *

ABSTRACT: The unique swimming strategies of natural microorganisms have inspired recent development of magnetic micro/nanorobots powered by artificial helical or flexible flagella. However, as artificial nanoswimmers with unique geometries are being developed, it is critical to explore new potential modes for kinetic optimization. For example, the freestyle stroke is the most efficient of the competitive swimming strokes for humans. Here we report a new type of magnetic nanorobot, a symmetric multilinked two-arm nanoswimmer, capable of efficient “freestyle” swimming at low Reynolds numbers. Excellent agreement between the experimental observations and theoretical predictions indicates that the powerful “freestyle” propulsion of the two-arm nanorobot is attributed to synchronized oscillatory deformations of the nanorobot under the combined action of magnetic field and viscous forces. It is demonstrated for the first time that the nonplanar propulsion gait due to the cooperative “freestyle” stroke of the two magnetic arms can be powered by a plane oscillatory magnetic field. These two-arm nanorobots are capable of a powerful propulsion up to 12 body lengths per second, along with on-demand speed regulation and remote navigation. Furthermore, the nonplanar propulsion gait powered by the consecutive swinging of the achiral magnetic arms is more efficient than that of common chiral nanohelical swimmers. This new swimming mechanism and its attractive performance opens new possibilities in designing remotely actuated nanorobots for biomedical operation at the nanoscale. KEYWORDS: Nanorobot, magnetic actuation, synchronized oscillation, nonplanar propulsion, kinetic optimization these flagella hydrodynamics for their propulsion.14,24−34 However, efficient propulsion gaits at the nanoscale are still quite limited. In his famous article “Life at low Reynolds number”, Purcell outlined a new three-link swimmer, comprised of three slender rods connected with two joints, which is essentially a simple discrete flagellum.35 In recent studies, Nelson’s group and Wang’s group have demonstrated the undulatory locomotion of similarly fashioned multilink magnetic nanoswimmers.36,37 The development of new efficient nanoswimmers requires critical evaluation of all potential modes of actuation.38 For example, humans have fixed shapes but are capable of a wide range of swimming motions, such as freestyle, breaststroke, or butterfly. Of these forms, freestyle has been found to offer the fastest motion possible through kinematic optimization. Similar analysis directed toward microand nanoswimmers would allow researchers to focus their efforts on the most viable propulsion mechanisms. Here we introduce a novel propulsion strategy based on a powerful “freestyle” swimming motion in response to an oscillating magnetic field. The new multilink two-arm artificial

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obotics deals with automated machines that can propel themselves and perform different tasks in various environments across different scales.1−11 Recent strides in micro- and nanofabrication technology have enabled researchers to design and develop highly capable micro- and nanoscale robotic systems for a growing number of medical applications.12,13 These versatile robots, on the order of micrometers or lower, are highly promising for traversing biological tissue and are capable of localized diagnostics and treatment with remarkable specificity and efficacy.14−18 It is therefore of particular importance to develop micro- and nanoswimmers capable of rapidly propelling and accurately reaching the desired location. However, in these low Reynolds number environments, conventional propulsion strategies break down due to prominent viscous forces, which require new specialized swimming techniques. Unicellular living organisms have a particularly distinctive way to achieve efficient motion in such environments. Natural microorganisms generally utilize either a set of flexible flagella or rigid flagella to propagate planar or helical traveling waves, respectively. These natural swimming strategies have inspired the development of micro/nanorobots powered by artificial helical or flexible flagella.1,19−23 Considerable attention has been directed toward engineering microswimmers that utilize © XXXX American Chemical Society

Received: June 5, 2017 Revised: July 4, 2017 Published: July 5, 2017 A

DOI: 10.1021/acs.nanolett.7b02383 Nano Lett. XXXX, XXX, XXX−XXX

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Figure 1. Design and fabrication of two-arm magnetic nanoswimmers. (a) Schematic of two-arm nanoswimmers. Applying an oscillating magnetic field on z-direction leads to freestyle swimming of the nanorobot with two nanoarms wobbling alternatively to generate actuation in the x−y-plane. (b) Scheme showing the fabrication process of two-arm nanoswimmers: (I) electrochemical deposition of the Ni−Ag−Au−Ag−Ni segments in AAO membrane, (II) dissolution the membrane and release the of the nanorods, and (III) etching the silver segment as deformable joints using hydrogen peroxide to obtain the two-arm nanoswimmer. (c) SEM image of a two-arm nanoswimmer and the corresponding energy-dispersive X-ray spectroscopy (EDX) mapping of elements Au, Ag, and Ni in the two-arm nanoswimmer. Scale bar, 500 nm.

nanoswimmer consists of a central gold body segment and two nickel arm segments connected by flexible porous silver hinges. Remarkably, in response to a planar oscillating magnetic field, the two-arm nanorobot exhibits an efficient nonplanar freestyle stroke, where the two arms swing cooperatively to push the middle link forward. The excellent agreement obtained between the experimental observations and the theoretical predictions confirms that this powerful freestyle gait is a result of the synchronized oscillatory deformation of the nanorobot under the combined action of magnetic field and viscous forces. Such freestyle swimming powered by an oscillating planar magnetic field is significantly more efficient than propulsion of existing helical (rigid or flexible) nanoswimmers driven by a rotating magnetic field. The powerful propulsion of the two-arm nanoswimmer demonstrates that kinematic optimization of nanoscale locomotion could be achieved by the new propulsion mode, while the propulsion driven by consecutive swinging of achiral bowed magnetic arms can be as efficient as chiral-driven propulsion in accordance with earlier theoretical predictions.39 This novel fuel-free freestyle nanoswimmer is thus expected to advance rapidly toward practical biomedical applications. Figure 1a illustrates the design of the two-arm nanoswimmer as well as the approach used for achieving freestyle strokes under an external oscillating magnetic field. The nanoswimmers consist of two magnetic metallic nanowire arms, and a gold metallic body, which are connected by flexible Ag hinges essential for generating periodic body deformations under an external oscillating magnetic field. As shown in the fabrication process of Figure 1b, the multilinked two-arm nanorobot are readily prepared with a template electrodeposition approach. The preparation involves sequential electrochemical deposition of the Ni, Ag, Au, Ag, and Ni segments into the 200 nm diameter nanopores of a thin membrane of porous anodic alumina. Dissolution of the alumina template releases the

multisegment nanowires, and the subsequent partial dissolution of the silver segment in hydrogen peroxide creates the porous Ag hinges. The resulting Ag hinges are essential for bending the nanoarms to generate nonreciprocal strokes. This fabrication strategy enables the construction of flexible structures with tailored length and desired components. The hinge length can be tuned to adjust the flexibility of the chain. The scanning electron microscopy (SEM) image of Figure 1c displays a twoarm nanoswimmer structure, consisting of two magnetic Ni arms with a length of ∼1.3 μm, one ∼1.3 μm long Au body, and two flexible Ag joints with a length of ∼0.6 μm. The Ni, Au, and Ag compositions of the nanorobot are further confirmed by the corresponding energy-dispersive X-ray spectroscopy (EDX) mapping (Figure 1c). The nanoswimmers are actuated through the application of an oscillating magnetic field (Figure 2a), which was generated using two sets of opposing electromagnetic coil pairs situated with a 180° phase shift. The dynamic body deformation of the nanorobot over 0.15 s is displayed in Figure 2b. Figure 2c shows the resulting continuous motion of a two-arm nanoswimmer via an external field with a frequency of 17 Hz over a 3 s period (taken from corresponding to SI Video 1). The speed of the nanorobot is 38.7 μm/s (∼8 body length/s) at the frequency of 17 Hz. Notably, the swimmer’s magnetic Ni arms continuously align with the orientation of the input field due to the exerted torque, while the whole swimmer body exhibits a forward motion. The oscillating magnetic field creates a wobbling of both magnetic arms. The nanoporous Ag’s elasticity allows the arm to flex during each stroke, thereby breaking the time-reversibility of the motion. To investigate the mechanism of freestyle nanoswimmer, we assume that the short flexible links made of porous silver can be modeled as elastic joints. The middle Au link of length l and the two Ni arms of length L are assumed to be rigid rods. B

DOI: 10.1021/acs.nanolett.7b02383 Nano Lett. XXXX, XXX, XXX−XXX

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Figure 2. Freestyle propulsion of two-arm nanoswimmer with an oscillating magnetic field. (a) Schematic showing the magnetic setup for propulsion along with the vibrating magnetic field. (b) Time lapse images (from SI Video 1) depicting the efficient propulsion of a freestyle nanoswimmer (magnetic frequency: 17 Hz). Scale bar, 2 μm. (c) Tracking lines (from SI Video 1) illustrating the travel distances of the freestyle nanoswimmer over 1, 2 and 3 s. Scale bar, 2 μm. (d) Dynamics of two-arm nanoswimmer and its shapes in different planes.

friction) and rotates with a somewhat different angular velocity. Propulsion in the vicinity of the surface breaks the symmetry of the nanoswimmer movement in the x−y-plane, leading to the in-sync (with the field frequency) oscillations. As a result, the motion of each arm resembles in-sync wobbling driven by a rotating magnetic field. Rotational dynamics of slender magnetic propellers steered by a rotating magnetic field is well understood:41 at low frequency of the actuating field, they tumble in the plane of the field rotation in-sync with the field; at some actuation frequency ωt‑w, the tumbling switches to in-sync wobbling, whereas the precession angle (i.e., the angle between the field rotation axis and the propeller’s easy-rotation axis) diminishes as driving frequency increases. At the so-called step-out frequency ωs‑o the magnetic torque exerted on the propeller can no longer counterbalance the increased viscous torque and the synchronous regime switches to the asynchronous one. Typically, insync wobbling regime is accompanied by a considerable propulsive motion. The Ni−Ag−Au structure bends under the action of magnetic torque and viscous stresses and adopts the arc-like shape. Magnetized rigid arc-shaped objects have been recognized as rather efficient propellers, exhibiting propulsion speeds comparable to these of magnetic helix. The propulsion velocity of such arc-shaped object in the in-sync wobbling regime reads39

Magnetization of the Ni arms is acquired in process of the nanoswimmer actuation in the external magnetic field H and their magnetic moments assumed to be equal to m1 and m2, respectively. The field oscillates along z-axis leading to oscillatory deformation of nanoswimmer in the x−z-plane as shown in Figure 1a. Because the magnetic moments m1 and m2 of both arms tend to align with the magnetic field H parallel to z-axes, they oscillate in an antiphase manner resulting in S-like shape of the nanoswimmer in the x−z-plane owing to finite elasticity of the joints (Figure 2d). Now we address the deformation in the x−y-plane. As it can be seen in experiments, there is also a permanent bending of the nanoswimmer arms in the x−y-plane perpendicular to the oscillating magnetic field in the direction opposite to the direction of propulsion. We choose y-axis as a direction of nanoswimmer propulsion and assume that both arms of the nanoswimmer are bent with the same (on average) angle ϕ with respect to the middle link as shown in Figure 2d. The original cause of this bending is probably the weak magnetic field gradient directed toward the center line of the electromagnetic coils. Such gradient results in the volumetric force f m = χ∇(H2), where χ is the magnetic susceptibility,40 and the corresponding weak magnetic torques bending the arms toward the center line of the coils. This weak bending is further enhanced owing to viscous forces exerted on the arms once the nanoswimmer is set into motion in the y-direction. Thus, in the x−y-plane the nanoswimmer adopts a Π-like shape (Figure 2d). It is important to notice that with each stroke of the magnetic arms with the external magnetic field, the middle link does not stay aligned with x-axis, but undergoes oscillations with respect to x-axis (SI Video 1). These oscillations might be attributed to alternating arm strokes in the vicinity of the surface. The estimated distance of the inactive nanowire from the bottom of the cell is d = kBT/mg ∼ 200−300 nm (sedimentation height); however, once the actuating field is turned on, the nanowire starts to hover above the surface at distance ∼1.5−2 μm due to the stretch of the arm and the flexible link. With the field switching, each arm experiences slightly different viscous forces (arm swinging against the surface experiences higher viscous

Usync = ωl

͠ ωt ‐ w 2Ch ωs2‐ o − ωt2‐ w

⎡ ω2 ⎤ ⎢1 − t ‐2w ⎥ ω ⎦ ⎣

(1)

͠ is the soHere l is the characteristic length of the filament, Ch ͠ called pseudochirality coefficient (typically Ch < 0.1). In the asynchronous regime beyond the step-out, ω > ωs‑o, the average propulsion velocity in eq 1 is reduced by a frequencydependent multiplicative factor41

⎡ Uasync = Usync⎢1 − ⎢⎣ C

1−

⎤ ωs2‐ o ⎥ ω 2 ⎥⎦

(2) DOI: 10.1021/acs.nanolett.7b02383 Nano Lett. XXXX, XXX, XXX−XXX

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Here C is the fitting constant independent of the liquid properties. Equations 5 and 6 describe the velocity of the Ni− Ag−Au structure toward the magnetic Ni-arm (see Figure 2d). The propulsion velocity of the nanoswimmer (in both the insync and a-sync regimes) composed of two conjugated Ni− Ag−Au structures follows from eqs 5 and 6 by multiplying by sine of the bending angle ϕ. Therefore, to find the velocity of the freestyle nanoswimmer one should determine the bending angle ϕ. On average, the nanoswimmer propels in the x−y-plane perpendicular to the oscillating magnetic field. Let u = (0, u, 0) be the net propulsion velocity. This motion results in drag force exerted on each arm. According to the resistive force theory the normal component f⊥ of the drag force per unit length is f⊥ = ς⊥(u·n)n, where ς⊥ is the drag coefficient of transverse motion and n is the unit vector normal to one arm. This drag force gives rise to the viscous torque (Figure 2d). The angle ϕ of the arms bending relative to the central link is found from the 1 balance of viscous and elastic torques, 2 uς⊥L2 cos ϕ = Kϕ, where K is the elasticity constant. Substituting u = U sin ϕ and introducing umin = 2K/(ς⊥L2), we obtain the equation that governs the bending angle ϕ in a self-consistent fashion

Notice that a single Ni arm connected to the Au middle link via the flexible Ag filament closely resembles the arc shape (Figure 2b). The major difference between the arc studied,39 and the arc-shaped Ni−Ag−Au structure is the flexibility of the ͠ , ωt‑w latter. It means that the parameters of the problem, i.e., Ch and ωs‑o, are not fixed, but depend on the actuating frequency. For elongated body, the tumbling-to-wobbling transition takes place at small enough frequency ωt‑w.41 At such frequencies the Ni−Ag−Au structure can be considered as a straight filament. The explicit relation for the tumbling-towobbling transition frequency reads ωt − w =

mH κ⊥

(3)

where m∥ is the longitudinal magnetic moment of the body and κ⊥ is the transverse viscous rotational friction coefficient. Our estimate of tumbling-to-wobbling transition frequency gives ωt‑w = 87 s−1 or νt‑w = ωt‑w/(2π) ≈ 14 Hz (see SI for details). In the experiments propulsion in three different liquids have been examined, seawater, cell culture medium solution, and serum solution, with viscosities 0.9, 1.1, and 1.6 cP, respectively. For the tumbling-to-wobbling frequency of three samples, we use the values 10, 8.2, and 5.5 Hz, correspondingly. The transition frequency of 10 Hz is the fitted, while the two other values are derived using the viscosity ratios. The explicit relation for the step-out frequency is given by41

ωs ‐ o =

m⊥H κ

U sin ϕ cos ϕ = uminϕ

where U is the propulsion velocity in both synchronous and asynchronous regimes. Physically, umin is the minimal velocity of the freely suspended Ni−Ag−Au flexible structure when the nontrivial inclination angle ϕ > 0 emerges. In seawater with η = 0.89 cP, we estimate umin = 10 μm s−1 (see SI for details). Similarly, for medium and serum we obtain umin = 8.2 and 5.5 μm s−1, respectively. Figure 3a, taken from SI Video 2, displays the moving trajectories of a freestyle nanoswimmer with magnetic field frequencies turning from 5 to 45 Hz, over a period of 1 s. The experimental speeds of the freestyle nanorobots in each experimental medium initially increase upon raising the input frequency of the oscillating magnetic field (Figure 3b). At the frequency of 5 Hz in water, the speed is 10.8 μm s−1, which is still significantly higher than Brownian diffusion. The freestyle nanorobot attains its fastest speed of 59.6 μm s−1 in water using a frequency of 25 Hz, with slower speeds observed at higher frequencies. At frequencies higher than the step-out frequency, the maximum available magnetic torque is insufficient to overcome the fluidic drag, leading to deceleration as the freestyle nanorobot moves out-of-sync with the applied magnetic field. The resulting system of eqs 7 and 5 is solved numerically with the indicated values of the parameters νt‑w, νs‑o and umin and the fitting constant C = 16.4 μm. The numerical speeds of the freestyle nanorobot under different magnetic field frequencies, shown also in Figure 3b, match well with the experimental results under the step-out frequency for each medium. Therefore, tuning the magnetic field enables rapid acceleration and deceleration of the freestyle nanoswimmer with precise speed control. Figure 4a, along with corresponding SI Video 3, displays the speed of a nanorobot in response to a square wave input over a 4 s period. At the frequency of 15 Hz, the nanoswimmer moves with a speed of 30.6 μm/s. An even more efficient propulsion with a speed of ∼60 μm/s is observed at the frequency of 25 Hz. Figure 4b tracks the time-dependence of the nanorobot speed upon switching the frequency repeatedly between 15 and 25 Hz. This time-lapse image demonstrates that the freestyle

(4)

where κ∥ is the viscous rotational resistance along the easy-axis of rotation and m⊥ is the transverse magnetic moment of the object. The step-out frequency ωs‑o is the maximal frequency in the synchronous regime. For a flexible magnetic object, its value cannot be estimated in a simple manner as ωt‑w because at elevated frequencies the filament deforms continuously so that m⊥ and κ∥ themselves are not fixed but vary with actuation frequency. When matching the experimental results to the theory, we use the value of 25 Hz for νs‑o = ωs‑o/(2π) for all suspending media. ͠ , can be determined The coefficient of pseudochirality, Ch ͠ is due to unambiguously only for rigid objects. Generally, Ch the arclike form of the filament. There are two main reasons for this form. First, the filament is slightly curved just after Ag dissolution (Figure 1c). Second, it is deformed owing to interaction of magnetized arms with external magnetic field. For a flexible nanoswimmer one can argue that the viscous stresses should diminish the filament deformations approaching a ͠ is proportional straight cylinder-like shape. We assume that Ch to characteristic deformations. Because the latter are determined by the balance of the elastic, magnetic, and viscous stresses, one can expect that the deformations are inversely ͠ ∼ 1/ηω. Using eqs 1 proportional to the viscous stresses, so Ch and 2, we find the following dependencies of the nanoswimmer velocity in synchronous and asynchronous regimes Usync = C

νt ‐ w νs2‐ o − νt2‐ w

⎡ Uasync = Usync⎢1 − ⎢⎣

⎡ ν2 ⎤ ⎢1 − t ‐2w ⎥ ν ⎦ ⎣

(5)

⎤ νs2‐ o ⎥ ν 2 ⎥⎦

(6)

1−

(7)

D

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Figure 3. Swimming performance of freestyle nanoswimmer under different magnetic frequencies. (a) Tracking lines (from SI video 2) illustrating the travel distances of freestyle nanoswimmer over a 1 s period in the presence of an oscillating magnetic field with a frequency of 5 (I), 15 (II), 25 (III), 35 (IV), and 45 Hz (V). Scale bar, 5 μm. (b) Experimental and calculated freestyle nanoswimmer speeds upon varying the magnetic frequency from 5 to 45 Hz in seawater (blue), medium (red), and serum (pink) solutions.

Figure 4. On-demand speed modulation and control of the freestyle nanoswimmers: (a) Velocity modulation of the freestyle nanoswimmers in response to a 1 s 15 Hz−25 Hz−15 Hz−25 Hz step. (b) Time-lapse images (from SI video 3) showing the velocity modulation of the freestyle nanoswimmers. Scale bar 5 μm. (c) Quantitative velocity of the freestyle nanoswimmers at different frequencies using oscillating magnetic field generated by square wave, triangle wave and sine wave. (d) Quantitative velocity of the freestyle nanoswimmers with different length arms (long arms, Ni, 1.3 μm; short arms, Ni, 0.8 μm) in different media at the frequency of 15 Hz. (e) Scheme of the magnetic control of freestyle nanoswimmers. (f) Time-lapse images showing the magnetically guided propulsion of freestyle nanoswimmer in the frequency of 15 Hz over 20 s. Scale bar 5 μm.

nanoswimmer displays an instantaneous switching between different frequencies with steady-state speeds reaching rapidly upon switching the frequency. The effect of driving signal of the oscillating magnetic field on the speed of freestyle nanoswimmer has also been investigated experimentally. As shown in Figure 4c, the different driving signals (square wave, triangle wave, and sine wave) have minimal effect on the motion of freestyle nanoswimmer. To evaluate the critical role of the geometric parameters, such as arm length, on the propulsive efficiency, freestyle nanoswimmers with different arm lengths were fabricated and tested in different solutions. The speeds of freestyle nanoswimmers with longer (1.3 μm) arm are 34.8, 19.8, and 12.6 μm/s in seawater, medium, and serum solution, respectively. These speeds are larger than the speeds of freestyle nanoswimmers with shorter (0.8 μm) arm. These data indicate that freestyle nanoswimmers with longer arms are capable of more efficient propulsion at the low Reynolds number. The longer arms possess a higher magnetic moment while the longitudinal rotational resistance increases only marginally, so that the step-out frequency shifts toward higher frequency. Thus, the propulsion velocity of the nanoswimmer with longer arms at the step-out is higher than that of the shorter-armed counterpart. Figure 4e,f presents the magnetic control of the directionality of the freestyle nanoswimmer. We observed that by changing the relative position between the electromagnet and the nanorobot in the x−y-plane, the directionality of the nanoswimmer could be tuned. As indicated in Figure 4e, the nanorobot always tends to move away from the line of centers of the electromagnets in the x−y-plane. This is due to weak gradient of the actuating field in the x−y-plane resulting in arm bending toward centerline of the coils as explained above.

Given that swinging of the bowed arms yields propulsion in the direction opposite to their bending, the nanoswimmer is always moving away from centerline of the electromagnets. Thus, by relocating the electromagnets to change their center projection point in the x−y-plane, the propulsion direction of the magnetic nanorobot could be altered. Figure 4f displays such real-time steering the freestyle nanorobot by relocating the electromagnets. Future efforts could lead to a more advanced control using multiple electromagnet pairs in the 3D space. Magnetic propulsion is highly promising for powering biomedical micro/nanorobots due to its noninvasive remote actuation and convenient navigation abilities. Recent advances in micro/nanofabrication has led to the successful engineering of bioinspired helical propellers and flexible-body propellers that replicate bacterial hydrodynamics. Here, we have presented a two-arm nanorobot that achieves a high-speed “freestyle” swimming motion, a new microscale propulsion mode that has not been observed in nature. This nanoswimmer, composed of Ni nanorods linked by an Au nanowire body with flexible Ag joints, exhibits synchronized nonplanar “freestyle” propulsion under a planar oscillating magnetic field. Our analytical modeling verifies that the observed propulsion is due to the synchronized oscillation of the nanorobot under the influence of the alternating magnetic field. In previous studies, the planar oscillating magnetic field could yield planar (wave-like) E

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Nano Letters deformations of a flexible filament.34,35 In this work, for the first time the “oscillating” magnetic field mimics the action of a “rotating” field, demonstrating that a planar oscillatory field is able to power nonplanar propulsion stroke resembling freestyle swimming. The speed and the direction of the nanorobot can be remotely modulated by adjusting the magnetic field with a maximum speed of 59.6 μm s−1, corresponding to a relative speed of ∼12 body lengths/second. Such efficient swimming indicates that propulsion driven by the cooperative out-of-phase wobbling of the pseudochiral bowed arms can be more efficient than the rotation-driven propulsion of chiral nano/microhelices. This efficient propulsion mechanism of the two-arm nanorobot holds considerable promise for a wide range of practical applications from nanoscale manipulation and assembly to nanomedicine. We also envision that the presented innovative nanorobotic design, which has not been observed in natural microorganisms, would inspire even more powerful locomotion strategies at the nanoscale.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nanolett.7b02383. Experimental methods, modeling about freestyle nanoswimmers (PDF) Freestyle propulsion of nanoswimmers (MPG) Swimming performance of freestyle nanoswimmers under different magnetic frequencies (MPG) On-demand speed modulation of a freestyle nanoswimmer (MPG) Motion control of a freestyle nanoswimmer (MPG)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. *E-mail: [email protected]. ORCID

Joseph Wang: 0000-0002-4921-9674 Author Contributions ∥

T.L.and J.L. contributed equally to this work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This project received support from the Defense Threat Reduction Agency-Joint Science and Technology Office for Chemical and Biological Defense (Grant HDTRA1-14-1-0064) National Natural Science Foundation of China (51521003 and 51175129), Key Laboratory of Microsystems and Microstructures Manufacturing of Ministry of Education (2016KM004). This work was supported in part by the Israel Ministry for Immigrant Absorption (K.I.M.).

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REFERENCES

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