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

R obotics deals with automated machines that can propel

themselves and perform different tasks in various
environments across different scales.1−11 Recent strides in
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
micro- and nanofabrication technology have enabled research- number”, Purcell outlined a new three-link swimmer,
ers to design and develop highly capable micro- and nanoscale comprised of three slender rods connected with two joints,
robotic systems for a growing number of medical applica- which is essentially a simple discrete flagellum.35 In recent
tions.12,13 These versatile robots, on the order of micrometers studies, Nelson’s group and Wang’s group have demonstrated
or lower, are highly promising for traversing biological tissue the undulatory locomotion of similarly fashioned multilink
and are capable of localized diagnostics and treatment with magnetic nanoswimmers.36,37 The development of new efficient
remarkable specificity and efficacy.14−18 It is therefore of nanoswimmers requires critical evaluation of all potential
particular importance to develop micro- and nanoswimmers modes of actuation.38 For example, humans have fixed shapes
capable of rapidly propelling and accurately reaching the but are capable of a wide range of swimming motions, such as
desired location. However, in these low Reynolds number freestyle, breaststroke, or butterfly. Of these forms, freestyle has
environments, conventional propulsion strategies break down been found to offer the fastest motion possible through
due to prominent viscous forces, which require new specialized kinematic optimization. Similar analysis directed toward micro-
swimming techniques. and nanoswimmers would allow researchers to focus their
Unicellular living organisms have a particularly distinctive efforts on the most viable propulsion mechanisms.
way to achieve efficient motion in such environments. Natural Here we introduce a novel propulsion strategy based on a
microorganisms generally utilize either a set of flexible flagella powerful “freestyle” swimming motion in response to an
or rigid flagella to propagate planar or helical traveling waves, oscillating magnetic field. The new multilink two-arm artificial
respectively. These natural swimming strategies have inspired
the development of micro/nanorobots powered by artificial Received: June 5, 2017
helical or flexible flagella.1,19−23 Considerable attention has Revised: July 4, 2017
been directed toward engineering microswimmers that utilize Published: July 5, 2017

© 2017 American Chemical Society 5092 DOI: 10.1021/acs.nanolett.7b02383

Nano Lett. 2017, 17, 5092−5098
Nano Letters Letter

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 multisegment nanowires, and the subsequent partial dissolution
nickel arm segments connected by flexible porous silver hinges. of the silver segment in hydrogen peroxide creates the porous
Remarkably, in response to a planar oscillating magnetic field, Ag hinges. The resulting Ag hinges are essential for bending the
the two-arm nanorobot exhibits an efficient nonplanar freestyle nanoarms to generate nonreciprocal strokes. This fabrication
stroke, where the two arms swing cooperatively to push the strategy enables the construction of flexible structures with
middle link forward. The excellent agreement obtained between tailored length and desired components. The hinge length can
the experimental observations and the theoretical predictions be tuned to adjust the flexibility of the chain. The scanning
confirms that this powerful freestyle gait is a result of the electron microscopy (SEM) image of Figure 1c displays a two-
synchronized oscillatory deformation of the nanorobot under arm nanoswimmer structure, consisting of two magnetic Ni
the combined action of magnetic field and viscous forces. Such arms with a length of ∼1.3 μm, one ∼1.3 μm long Au body, and
freestyle swimming powered by an oscillating planar magnetic two flexible Ag joints with a length of ∼0.6 μm. The Ni, Au,
field is significantly more efficient than propulsion of existing and Ag compositions of the nanorobot are further confirmed by
helical (rigid or flexible) nanoswimmers driven by a rotating the corresponding energy-dispersive X-ray spectroscopy (EDX)
magnetic field. The powerful propulsion of the two-arm mapping (Figure 1c).
nanoswimmer demonstrates that kinematic optimization of The nanoswimmers are actuated through the application of
nanoscale locomotion could be achieved by the new propulsion an oscillating magnetic field (Figure 2a), which was generated
mode, while the propulsion driven by consecutive swinging of using two sets of opposing electromagnetic coil pairs situated
achiral bowed magnetic arms can be as efficient as chiral-driven with a 180° phase shift. The dynamic body deformation of the
propulsion in accordance with earlier theoretical predictions.39 nanorobot over 0.15 s is displayed in Figure 2b. Figure 2c
This novel fuel-free freestyle nanoswimmer is thus expected to shows the resulting continuous motion of a two-arm nano-
advance rapidly toward practical biomedical applications. swimmer via an external field with a frequency of 17 Hz over a
Figure 1a illustrates the design of the two-arm nanoswimmer 3 s period (taken from corresponding to SI Video 1). The
as well as the approach used for achieving freestyle strokes speed of the nanorobot is 38.7 μm/s (∼8 body length/s) at the
under an external oscillating magnetic field. The nanoswimmers frequency of 17 Hz. Notably, the swimmer’s magnetic Ni arms
consist of two magnetic metallic nanowire arms, and a gold continuously align with the orientation of the input field due to
metallic body, which are connected by flexible Ag hinges the exerted torque, while the whole swimmer body exhibits a
essential for generating periodic body deformations under an forward motion. The oscillating magnetic field creates a
external oscillating magnetic field. As shown in the fabrication wobbling of both magnetic arms. The nanoporous Ag’s
process of Figure 1b, the multilinked two-arm nanorobot are elasticity allows the arm to flex during each stroke, thereby
readily prepared with a template electrodeposition approach. breaking the time-reversibility of the motion.
The preparation involves sequential electrochemical deposition To investigate the mechanism of freestyle nanoswimmer, we
of the Ni, Ag, Au, Ag, and Ni segments into the 200 nm assume that the short flexible links made of porous silver can be
diameter nanopores of a thin membrane of porous anodic modeled as elastic joints. The middle Au link of length l and the
alumina. Dissolution of the alumina template releases the two Ni arms of length L are assumed to be rigid rods.
5093 DOI: 10.1021/acs.nanolett.7b02383
Nano Lett. 2017, 17, 5092−5098
Nano Letters Letter

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.

Magnetization of the Ni arms is acquired in process of the friction) and rotates with a somewhat different angular velocity.
nanoswimmer actuation in the external magnetic field H and Propulsion in the vicinity of the surface breaks the symmetry of
their magnetic moments assumed to be equal to m1 and m2, the nanoswimmer movement in the x−y-plane, leading to the
respectively. The field oscillates along z-axis leading to in-sync (with the field frequency) oscillations. As a result, the
oscillatory deformation of nanoswimmer in the x−z-plane as motion of each arm resembles in-sync wobbling driven by a
shown in Figure 1a. Because the magnetic moments m1 and m2 rotating magnetic field.
of both arms tend to align with the magnetic field H parallel to Rotational dynamics of slender magnetic propellers steered
z-axes, they oscillate in an antiphase manner resulting in S-like by a rotating magnetic field is well understood:41 at low
shape of the nanoswimmer in the x−z-plane owing to finite frequency of the actuating field, they tumble in the plane of the
elasticity of the joints (Figure 2d). field rotation in-sync with the field; at some actuation frequency
Now we address the deformation in the x−y-plane. As it can ωt‑w, the tumbling switches to in-sync wobbling, whereas the
be seen in experiments, there is also a permanent bending of precession angle (i.e., the angle between the field rotation axis
the nanoswimmer arms in the x−y-plane perpendicular to the and the propeller’s easy-rotation axis) diminishes as driving
oscillating magnetic field in the direction opposite to the frequency increases. At the so-called step-out frequency ωs‑o the
direction of propulsion. We choose y-axis as a direction of magnetic torque exerted on the propeller can no longer
nanoswimmer propulsion and assume that both arms of the counterbalance the increased viscous torque and the synchro-
nanoswimmer are bent with the same (on average) angle ϕ nous regime switches to the asynchronous one. Typically, in-
with respect to the middle link as shown in Figure 2d. The sync wobbling regime is accompanied by a considerable
original cause of this bending is probably the weak magnetic propulsive motion.
field gradient directed toward the center line of the electro- The Ni−Ag−Au structure bends under the action of
magnetic coils. Such gradient results in the volumetric force f m magnetic torque and viscous stresses and adopts the arc-like
= χ∇(H2), where χ is the magnetic susceptibility,40 and the shape. Magnetized rigid arc-shaped objects have been
corresponding weak magnetic torques bending the arms toward recognized as rather efficient propellers, exhibiting propulsion
the center line of the coils. This weak bending is further speeds comparable to these of magnetic helix. The propulsion
enhanced owing to viscous forces exerted on the arms once the velocity of such arc-shaped object in the in-sync wobbling
nanoswimmer is set into motion in the y-direction. Thus, in the regime reads39
x−y-plane the nanoswimmer adopts a Π-like shape (Figure 2d). ͠ ωt ‐ w
2Ch ⎡ ω2 ⎤
It is important to notice that with each stroke of the magnetic Usync = ωl ⎢1 − t ‐2w ⎥
arms with the external magnetic field, the middle link does not ωs2‐ o − ωt2‐ w ⎣ ω ⎦ (1)
stay aligned with x-axis, but undergoes oscillations with respect
to x-axis (SI Video 1). These oscillations might be attributed to ͠ is the so-
Here l is the characteristic length of the filament, Ch
alternating arm strokes in the vicinity of the surface. The called pseudochirality coefficient (typically Ch ͠ < 0.1). In the
estimated distance of the inactive nanowire from the bottom of asynchronous regime beyond the step-out, ω > ωs‑o, the average
the cell is d = kBT/mg ∼ 200−300 nm (sedimentation height); propulsion velocity in eq 1 is reduced by a frequency-
however, once the actuating field is turned on, the nanowire dependent multiplicative factor41
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 ωs2‐ o ⎥
switching, each arm experiences slightly different viscous forces Uasync = Usync⎢1 − 1−
⎢⎣ ω 2 ⎥⎦ (2)
(arm swinging against the surface experiences higher viscous
5094 DOI: 10.1021/acs.nanolett.7b02383
Nano Lett. 2017, 17, 5092−5098
Nano Letters Letter

Notice that a single Ni arm connected to the Au middle link Here C is the fitting constant independent of the liquid
via the flexible Ag filament closely resembles the arc shape properties. Equations 5 and 6 describe the velocity of the Ni−
(Figure 2b). The major difference between the arc studied,39 Ag−Au structure toward the magnetic Ni-arm (see Figure 2d).
and the arc-shaped Ni−Ag−Au structure is the flexibility of the The propulsion velocity of the nanoswimmer (in both the in-
͠ , ωt‑w
latter. It means that the parameters of the problem, i.e., Ch sync and a-sync regimes) composed of two conjugated Ni−
and ωs‑o, are not fixed, but depend on the actuating frequency. Ag−Au structures follows from eqs 5 and 6 by multiplying by
For elongated body, the tumbling-to-wobbling transition sine of the bending angle ϕ. Therefore, to find the velocity of
takes place at small enough frequency ωt‑w.41 At such the freestyle nanoswimmer one should determine the bending
frequencies the Ni−Ag−Au structure can be considered as a angle ϕ.
straight filament. The explicit relation for the tumbling-to- On average, the nanoswimmer propels in the x−y-plane
wobbling transition frequency reads perpendicular to the oscillating magnetic field. Let u = (0, u, 0)
be the net propulsion velocity. This motion results in drag force
mH exerted on each arm. According to the resistive force theory the
ωt − w =
κ⊥ (3) 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
where m∥ is the longitudinal magnetic moment of the body and and n is the unit vector normal to one arm. This drag force
κ⊥ is the transverse viscous rotational friction coefficient. gives rise to the viscous torque (Figure 2d). The angle ϕ of the
Our estimate of tumbling-to-wobbling transition frequency arms bending relative to the central link is found from the
gives ωt‑w = 87 s−1 or νt‑w = ωt‑w/(2π) ≈ 14 Hz (see SI for 1
details). In the experiments propulsion in three different liquids balance of viscous and elastic torques, 2 uς⊥L2 cos ϕ = Kϕ,
have been examined, seawater, cell culture medium solution, where K is the elasticity constant. Substituting u = U sin ϕ and
and serum solution, with viscosities 0.9, 1.1, and 1.6 cP, introducing umin = 2K/(ς⊥L2), we obtain the equation that
respectively. For the tumbling-to-wobbling frequency of three governs the bending angle ϕ in a self-consistent fashion
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 U sin ϕ cos ϕ = uminϕ (7)
other values are derived using the viscosity ratios.
The explicit relation for the step-out frequency is given by41 where U is the propulsion velocity in both synchronous and
asynchronous regimes. Physically, umin is the minimal velocity
m⊥H of the freely suspended Ni−Ag−Au flexible structure when the
ωs ‐ o =
κ (4) nontrivial inclination angle ϕ > 0 emerges. In seawater with η =
0.89 cP, we estimate umin = 10 μm s−1 (see SI for details).
where κ∥ is the viscous rotational resistance along the easy-axis Similarly, for medium and serum we obtain umin = 8.2 and 5.5
of rotation and m⊥ is the transverse magnetic moment of the μm s−1, respectively.
object. The step-out frequency ωs‑o is the maximal frequency in Figure 3a, taken from SI Video 2, displays the moving
the synchronous regime. For a flexible magnetic object, its value trajectories of a freestyle nanoswimmer with magnetic field
cannot be estimated in a simple manner as ωt‑w because at frequencies turning from 5 to 45 Hz, over a period of 1 s. The
elevated frequencies the filament deforms continuously so that experimental speeds of the freestyle nanorobots in each
m⊥ and κ∥ themselves are not fixed but vary with actuation experimental medium initially increase upon raising the input
frequency. When matching the experimental results to the frequency of the oscillating magnetic field (Figure 3b). At the
theory, we use the value of 25 Hz for νs‑o = ωs‑o/(2π) for all frequency of 5 Hz in water, the speed is 10.8 μm s−1, which is
suspending media. still significantly higher than Brownian diffusion. The freestyle
The coefficient of pseudochirality, Ch ͠ , can be determined nanorobot attains its fastest speed of 59.6 μm s−1 in water using
unambiguously only for rigid objects. Generally, Ch ͠ is due to a frequency of 25 Hz, with slower speeds observed at higher
the arclike form of the filament. There are two main reasons for frequencies. At frequencies higher than the step-out frequency,
this form. First, the filament is slightly curved just after Ag the maximum available magnetic torque is insufficient to
dissolution (Figure 1c). Second, it is deformed owing to overcome the fluidic drag, leading to deceleration as the
interaction of magnetized arms with external magnetic field. For freestyle nanorobot moves out-of-sync with the applied
a flexible nanoswimmer one can argue that the viscous stresses magnetic field. The resulting system of eqs 7 and 5 is solved
should diminish the filament deformations approaching a numerically with the indicated values of the parameters νt‑w, νs‑o
straight cylinder-like shape. We assume that Ch ͠ is proportional and umin and the fitting constant C = 16.4 μm. The numerical
to characteristic deformations. Because the latter are speeds of the freestyle nanorobot under different magnetic field
determined by the balance of the elastic, magnetic, and viscous frequencies, shown also in Figure 3b, match well with the
stresses, one can expect that the deformations are inversely experimental results under the step-out frequency for each
͠ ∼ 1/ηω. Using eqs 1
proportional to the viscous stresses, so Ch medium. Therefore, tuning the magnetic field enables rapid
and 2, we find the following dependencies of the nanoswimmer acceleration and deceleration of the freestyle nanoswimmer
velocity in synchronous and asynchronous regimes with precise speed control.
Figure 4a, along with corresponding SI Video 3, displays the
νt ‐ w ⎡ ν2 ⎤ speed of a nanorobot in response to a square wave input over a
Usync = C ⎢1 − t ‐2w ⎥ 4 s period. At the frequency of 15 Hz, the nanoswimmer moves
νs2‐ o − νt2‐ w ⎣ ν ⎦ (5) 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
⎡ ⎤
νs2‐ o ⎥ Hz. Figure 4b tracks the time-dependence of the nanorobot
Uasync = Usync⎢1 − 1− speed upon switching the frequency repeatedly between 15 and
⎢⎣ ν 2 ⎥⎦ (6) 25 Hz. This time-lapse image demonstrates that the freestyle
5095 DOI: 10.1021/acs.nanolett.7b02383
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Nano Letters Letter

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 Figure 4. On-demand speed modulation and control of the freestyle
period in the presence of an oscillating magnetic field with a frequency nanoswimmers: (a) Velocity modulation of the freestyle nano-
of 5 (I), 15 (II), 25 (III), 35 (IV), and 45 Hz (V). Scale bar, 5 μm. (b) swimmers in response to a 1 s 15 Hz−25 Hz−15 Hz−25 Hz step.
Experimental and calculated freestyle nanoswimmer speeds upon (b) Time-lapse images (from SI video 3) showing the velocity
varying the magnetic frequency from 5 to 45 Hz in seawater (blue), modulation of the freestyle nanoswimmers. Scale bar 5 μm. (c)
medium (red), and serum (pink) solutions. 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
nanoswimmer displays an instantaneous switching between nanoswimmers with different length arms (long arms, Ni, 1.3 μm;
different frequencies with steady-state speeds reaching rapidly short arms, Ni, 0.8 μm) in different media at the frequency of 15 Hz.
upon switching the frequency. The effect of driving signal of the (e) Scheme of the magnetic control of freestyle nanoswimmers. (f)
oscillating magnetic field on the speed of freestyle nano- Time-lapse images showing the magnetically guided propulsion of
freestyle nanoswimmer in the frequency of 15 Hz over 20 s. Scale bar 5
swimmer has also been investigated experimentally. As shown μm.
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 Given that swinging of the bowed arms yields propulsion in the
geometric parameters, such as arm length, on the propulsive direction opposite to their bending, the nanoswimmer is always
efficiency, freestyle nanoswimmers with different arm lengths moving away from centerline of the electromagnets. Thus, by
were fabricated and tested in different solutions. The speeds of relocating the electromagnets to change their center projection
freestyle nanoswimmers with longer (1.3 μm) arm are 34.8, point in the x−y-plane, the propulsion direction of the
19.8, and 12.6 μm/s in seawater, medium, and serum solution, magnetic nanorobot could be altered. Figure 4f displays such
respectively. These speeds are larger than the speeds of real-time steering the freestyle nanorobot by relocating the
freestyle nanoswimmers with shorter (0.8 μm) arm. These data electromagnets. Future efforts could lead to a more advanced
indicate that freestyle nanoswimmers with longer arms are control using multiple electromagnet pairs in the 3D space.
capable of more efficient propulsion at the low Reynolds Magnetic propulsion is highly promising for powering
number. The longer arms possess a higher magnetic moment biomedical micro/nanorobots due to its noninvasive remote
while the longitudinal rotational resistance increases only actuation and convenient navigation abilities. Recent advances
marginally, so that the step-out frequency shifts toward higher in micro/nanofabrication has led to the successful engineering
frequency. Thus, the propulsion velocity of the nanoswimmer of bioinspired helical propellers and flexible-body propellers
with longer arms at the step-out is higher than that of the that replicate bacterial hydrodynamics. Here, we have presented
shorter-armed counterpart. a two-arm nanorobot that achieves a high-speed “freestyle”
Figure 4e,f presents the magnetic control of the directionality swimming motion, a new microscale propulsion mode that has
of the freestyle nanoswimmer. We observed that by changing not been observed in nature. This nanoswimmer, composed of
the relative position between the electromagnet and the Ni nanorods linked by an Au nanowire body with flexible Ag
nanorobot in the x−y-plane, the directionality of the nano- joints, exhibits synchronized nonplanar “freestyle” propulsion
swimmer could be tuned. As indicated in Figure 4e, the under a planar oscillating magnetic field. Our analytical
nanorobot always tends to move away from the line of centers modeling verifies that the observed propulsion is due to the
of the electromagnets in the x−y-plane. This is due to weak synchronized oscillation of the nanorobot under the influence
gradient of the actuating field in the x−y-plane resulting in arm of the alternating magnetic field. In previous studies, the planar
bending toward centerline of the coils as explained above. oscillating magnetic field could yield planar (wave-like)
5096 DOI: 10.1021/acs.nanolett.7b02383
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Nano Letters Letter

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