Flexible Guidance of Microengines by Dynamic Topographical

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Flexible Guidance of Microengines by Dynamic Topographical Pathways in Ferrofluids Fan Yang, Fangzhi Mou,* Yuzhou Jiang, Ming Luo, Leilei Xu, Huiru Ma, and Jianguo Guan* Downloaded via UNIV OF CALIFORNIA SANTA BARBARA on June 24, 2018 at 08:10:17 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

State Key Laboratory of Advanced Technology for Materials Synthesis and Processing, International School of Materials Science and Engineering, Wuhan University of Technology, Wuhan 430070, China S Supporting Information *

ABSTRACT: In this work, we demonstrate a simple, versatile, and real-time motion guidance strategy for artificial microengines and motile microorganisms in a ferrofluid by dynamic topographical pathways (DTPs), which are assembled from superparamagnetic nanoparticles in response to external magnetic field (H). In this general strategy, the DTPs can exert anisotropic resistance forces on autonomously moving microengines and thus regulate their orientation. As the DTPs with different directions and lengths can be reversibly and swiftly assembled in response to the applied H, the microengines in the ferrofluid can be guided on demand with controlled motion directions and trajectories, including circular, elliptical, straight-line, semi-sine, and sinusoidal trajectories. The asdemonstrated control strategy obviates reliance on the customized responses of micromotors and applies to autonomously propelling agents swimming both in bulk and near substrate walls. Furthermore, the microengines (or motile microorganisms) in a ferrofluid can be considered as an integrated system, and it may inspire the development of intelligent systems with cooperative functions for biomedical and environmental applications. KEYWORDS: micro/nanomotors, ferrofluids, topographical pathways, magnetic guidance magnetic field,24 light,25 gravity,26 flow,27,28 electric field29,30 and chemical gradient field,31,32 or topographical pathways, such as local micropatterns and microchannels on the substrate,33−35 to construct anisotropic environments. Consequently, the alignment of micro/nanomotors or the direction of driving forces is regulated, resulting in controlled motion directions and trajectories. Between them, the topographical pathways on the substrate can directly guide micro/nanomotors due to the profound effects of local boundaries or obstacles on the local product distribution, local flow fields, motor alignment, etc., obviating the need for external fields and customized micro/nanomotors.36,37 However, all the topographical pathways demonstrated so far are required to be sculptured on the substrates in advance, thus are incapable of guiding those autonomously propelling agents swimming in bulk, such as motile microorganisms, bubble-propelled spherical micromotors, and tubular microengines. More importantly, these topographical pathways are rigid and

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icro/nanomotors are micro/nanoscale devices capable of moving autonomously in liquid media by harvesting energy from surrounding chemical fuels or external fields (light, heat, ultrasound, electric, or magnetic field).1−3 These tiny devices are envisioned to revolutionize emerging topics in sensing, micro/nanoengineering, biomedicine, and environmental science.3 Over the past decade, various micro/nanomotors, such as Janus structured, pot-like, tubular, and isotropic micro/nanomotors have been developed based on the propulsion mechanism of bubble recoil and self-phoresis.4−21 Owing to the specific properties of the developed micro/nanomotors, they have shown great promises to perform complex tasks, such as drug delivery, microsurgery, sensing, cargo transport, and microfactories.1−3 To perform these tasks efficiently, it is of great significance to guide micro/ nanomotors in controlled motion directions and trajectories.22,23 The essential principle for the guidance of micro/nanomotors is to provide an anisotropic environment to regulate their alignments or control their driving-force directions. In the past decade, considerable efforts have been devoted to motion guidance of micro/nanomotors based on this principle. They mainly include the use of external stimuli, such as external © XXXX American Chemical Society

Received: March 5, 2018 Accepted: June 15, 2018 Published: June 15, 2018 A

DOI: 10.1021/acsnano.8b01682 ACS Nano XXXX, XXX, XXX−XXX

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Figure 1. (A) Schematic demonstration of a microengine in the ferrofluid with Fe3O4@PVP NPs. Without H, the microengine moves freely (left). When H is applied, the microengine is guided to move along the DTPs assembled from superparamagnetic Fe3O4@PVP NPs (right). (B) Time-lapse optical microscopic images illustrating the guidance of a microengine in the ferrofluid by the DTPs. The green curve is a trajectory of the microengine in 0.4 s before DTPs are assembled when H is off. Red curves represent the successive trajectories of the microengine guided by DTPs when H is applied. H with an intensity of 66 Gs was applied by a permanent NdFeB magnet. Scale bar in B, 20 μm.

unchangeable once sculptured, which makes it impossible to achieve flexible motion guidance of micro/nanomotors on demand. Ferrofluid is a colloid dispersion of magnetic particles within a liquid and has attracted considerable attentions in engineering, optic devices, and in vivo/in vitro biomedical applications.38 It may provide a desired anisotropic environment to guide micro/nanomotors thanks to the dynamic generation of one-dimensional (1D) particle chains within it in response to external magnetic fields.39−41 Recently, we have reported the ferrofluids with tunable structural colors based on monodispersed superparamagnetic Fe3O4@poly(vinylpyrrolidone) nanoparticles (Fe3O4@PVP NPs), which can be stably dispersed in liquids for a long time independent of their polarity, ionic strength, and pH value of the liquid owing to the steric repulsions, and reversibly assembled into paralleled 1D nanoparticle chains in response to external magnetic fields (H).42 In this work, we demonstrate that the magnetically responsive nanoparticle chains in ferrofluids can act as dynamic topographical pathways (DTPs), offering a flexible, versatile, and real-time control strategy to guide microengines on demand. The anisotropic resistances from DTPs ensure microengines to move along the pathways. As the DTPs are reversibly and swiftly formed upon the application of H with their length and direction depending on the intensity and direction of H, the motion directions of the microengine can be controlled in real time. In this way, microengines can be maneuvered on demand with various trajectories including circular, elliptical, straight-line, semi-sine, and sinusoidal ones. Besides artificial microengines, living cells are also demonstrated to be effectively guided by DTPs. The as-reported control strategy has significant advantages of flexibilities and simplicities and applies to microengines moving both in bulk and near substrate walls. In addition, the as-developed integrated aqueous system consisting of magnetic nanoparticles and microengines (or motile microorganisms) is expected to act as an intelligent system with cooperative

functions for biomedical and environmental applications.10,43−46

RESULTS AND DISCUSSION To demonstrate the flexible on-demand guidance of micromotors by dynamic topographical pathways (DTPs), we fabricated catalytic polypyrrole/Pt (PPy/Pt) tubular microengines (Figure S1A and B) by an electrochemical method and dispersed them in a ferrofluid with superparamagnetic Fe3O4@ PVP NPs (Figure S1C and D). The as-fabricated catalytic polypyrrole/Pt tubular microengines are nonmagnetic and possess strong driving forces, high stability, and easy operation in various aqueous media.42,48,49 Upon the application of an external magnetic field (H), the Fe3O4@PVP NPs in the ferrofluid are assembled into 1D nanoparticle chains as DTPs (Video S1). Compared with the rigid topographical pathways presculptured on substrates,33−37 the DTPs are not only stably suspended in media but also can be swiftly and reversibly assembled and disassembled in response to H. Hence, they can be employed to realize the flexible real-time guidance of micromotors swimming in bulk, for example, bubble-propelled tubular microengines, as demonstrated in the conceptual schematics in Figure 1A. The nonmagnetic catalytic polypyrrole/Pt tubular microengines in a ferrofluid with 8.5 wt % Fe3O4@PVP NPs show an efficient bubble propulsion frequently with circular and spiral trajectories if no H is applied (Figure 1B and Video S2), similar to those in an aqueous medium without Fe3O4@PVP NPs (Figure S2 and Video S3). This indicates that the presence of Fe3O4@PVP NPs in the medium has a negligible effect on the autonomous motions of the microengines if no H is applied. Upon the application of an H of 66 Gs by a permanent NdFeB magnet, the movement of the nonmagnetic microengine becomes parallel to DTPs after about 2 s (Figure 1B and Video S2). This proves that the DTPs can guide the nonmagnetic microengine as effective as the traditional B

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number of longitudinal gaps between chains, leading to incomplete DTPs. When the microengine meets a gap, it will jump the rails and move freely until it encounters other chains. The l of DTPs can be adjusted by the concentration of magnetic nanoparticles (Cp), the intensity of external magnetic field (H), and the H applied time (t).50 Figure S4 indicates that when an H of 66 Gs is on, l grows to 20.2 μm in 2.1 s and becomes stable at 20.8 μm after 2.5 s. Correspondingly, the microengine moves initially in a curved trajectory and then in a straight line along the DTPs when l ≥ 20.8 μm. Varying Cp from 10 to 94 mg/mL makes the average l of DTPs grow from 10.1 and 27.8 μm at a constant H of 66 Gs, as shown in Figure S5. Figure 3A and B illustrates that in a ferrofluid with Cp of 94 mg/mL and without H, the microengine shows a circular trajectory with a diameter of 34 μm. Under magnetic field, l increases with increasing H, and the circular trajectory of the microengine transforms into an elliptical one with a semimajor axis (a) parallel to the direction of nanoparticle chains (or the H direction) and increasing with l. Under an H of 66 Gs, l reaches to 27.8 μm at t over 10 s, and the motion trajectory of the microengine becomes a straight line along DTPs (Video S6). This implies that the motion trajectories of the microengine can be modulated from circular, elliptical to straight-line ones by controlling l under different H. The velocity of the microengine in the direction parallel to H and DTPs (vH) before it goes back can reflect the guidance efficacy by DTPs. Figure 3C shows that vH increases with increasing l. The average critical length (l*) of DTPs, which is defined as that can effectively guide microengines to move in a straightline trajectory, is calculated to be 22.7 μm according to experimental observations of l-dependent motions of microengines. In this DTP guidance strategy, the DTPs, even those formed at a low H, have an enough strong strength to withstand the crash of microengine. The strength of DTPs can be represented by the interparticle magnetic attractive force (Fmag). It is calculated to be 5.1 μN at 66 Gs and 0.25 μN at 22 Gs from eq 1:42,51 ÄÅ ÉÑ 2Ñ ÅÅ 4 3 ÅÅ πr ρM ÑÑÑ Å 3 ÑÑ ÑÑ Fmag = 6 × ÅÅÅÅ 4 ÑÑ ÅÅ d ÑÑ ÅÅ ÑÑÖ (1) ÅÇ

magnetic guidance of the magnetic microengine with nickel inclusions (Figure S3 and Video S4). As the most common and robust approach for the motion guidance, the traditional magnetic guidance requires micro/ nanomotors to possess a customized magnetic anisotropy by incorporating ferromagnetic materials into their bodies with sophisticated and expensive processing techniques.22,24,47,48 This, to some extent, hinders the large-scale production and application of magnetic micro/nanomotors. In addition, the incorporated magnetic materials are usually metal nickel, cobalt, or their alloys. They are easily corroded into toxic compounds in aqueous media with high ion concentration or low pH.49 In contrast, the as-demonstrated strategy of guiding microengine by DTPs is simply to carry out and friendly to systems. In the microengine guidance strategy by DTPs, the DTPs offer anisotropic resistances for the moving microengine. The interaction between a microengine and DTPs is illustrated in Figure 2A, in which F1 is the driving force from the ejected

Figure 2. (A) The forces acting on a microengine when it moves against a DTP. (B) Dark-field transmission optical microscopic images demonstrating the motion of a microengine in the medium containing two local regions with and without DTPs, respectively. H with an intensity of 66 Gs was applied by a permanent NdFeB magnet. Scale bar, 50 μm.

(

)

where r, ρ, and M (M = χH, where χ is the magnetic susceptibility) are the radius (75 nm), density (5.1 g/cm3), and mass magnetization (1.35 and 6.10 emu/g at 22 and 66 Gs, respectively) of the Fe3O4@PVP NPs, respectively, and d denotes the distance (245 nm) between the centers of nanoparticles. The propulsion force (Fjet) of the microengine is calculated to be 4.37 pN according to eq 2:52

bubbles, F2 is the force from a DTP, and f is the drag forces from the medium. The microengine receives a minimum resistance when it moves along DTPs. Otherwise, it will be subjected to force F2, which generates a torque to turn the microengine parallel to DTPs (Figure 2A). As the DTPs are parallel chains in three-dimension, the microengine will receive forces from all directions other than the DTP direction to regulate its motion along the DTPs. In order to further verify the guiding effect of DTPs on the microengine, we have observed the motion behaviors of a microengine in local regions with and without DTPs, respectively. As shown in Figure 2B and Video S5, the microengine moves in a straightline trajectory in the right region with DTPs and moves in a spiral trajectory in the left region once it crosses the border. This suggests the strong guiding effect of DTPs on its motions. The interaction between the microengine and DTPs (Figure 2A) further indicates that the guidance of the microengine strongly depends on the length (l) of DTPs. When the nanoparticle chains are not long enough, there are a large

2πμLv

Fjet = ln

( ) − 0.72 L R max

(2)

where L and Rmax are the length (10 μm) and maximum radius (1 μm) of the conical microengine, v is the motion speed of the microengine (110 μm/s), and μ is the dynamic viscosity of the medium (1 mPa s). This confirms that the propulsion force of the microengine is far weaker than the interparticle magnetic attractive force even at a low H of 22 Gs, and the microengine is difficult to break a DTP. In addition, at a low H, l of the formed DTPs is less than l*. In this case, the microengine could easily find a gap and slightly push DTPs away from their C

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Figure 3. (A) Dark-field and bright-field transmission optical microscopic images showing (top row) DTPs with different length (l) assembled under different H provided by a permanent NdFeB magnet and (bottom row) the motion trajectories of a microengine guided by the DTPs with different l in the ferrofluid. Scale bars, 20 μm. (B) l versus H. (C) The relationship between vH and l, in which the data points are taken as an average velocity of five moving microengines.

Figure 4. (A) Schematic illustration of the changes in motion directions of a microengine in the ferrofluid with the reorientation of DTPs under an H applied in different directions. (B) Dark-field transmission optical microscopic images of a microengine at different time, indicating that the microengine changes its motion directions with the orientation of DTPs. H (66 Gs) is provided by a permanent NdFeB magnet to control the orientation of DTPs. The green curve is a trajectory in 1.2 s of the microengine without DTPs guidance when H is off. Red curves are trajectories of the microengine guided by DTPs with varied orientations. Scale bar, 50 μm.

original locations rather than break a DTP, as shown in Figure S6. Hence, the guiding effect of DTPs on the microengine is mainly determined by l. The guidance of microengines depends not only on the length of DTPs but also on the orientation of DTPs. As shown in the conceptual schematics in Figure 4A, the motion direction of a microengine changes in real time with the orientation of the DTPs via changing the applied H. By successively changing the orientation of DTPs, the microengine can move along a designed path. Figure 4B displays

experimental time-lapse images and trajectories of a selfpropelled microengine in response to the orientation change of the DTPs. It is clear from the images that changing H direction will result in the corresponding change in the orientation of the DTPs, and subsequently change the motion direction and control the motion trajectory of the microengine. The rectangular trajectory of the microengine in Figure 4B manifests that it reaches the designated points (points a−d) in a sequential order at the time of 1.1, 2.6, 4, and 5.5 s, respectively (Video S7). D

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Figure 5. (A) Schematic illustration of the color change of DTPs with the tilting angle (θ) to z axis (the direction of the back scattered light) in x−z plane (y axis points into the screen). (B) The dark-field reflective optical microscopic images depicting the diffractive color changes of DTPs with different θ and the navigated motion of a microengine in z direction over time observed from x−y plane. Scale bar, 50 μm. (C) The time-lapse dark-field reflective optical microscopic images demonstrating that the microengine can approach and hit the substrate wall and then be trapped there under the guidance of the tilting DTPs. Scale bar, 20 μm. H = 130 Gs, provided by a permanent NdFeB magnet and Cp = 94 mg/mL.

Figure 6. (A) The optical microscopic image and motion trajectory (the red curve in 0.53 s) of a microengine in the ferrofluid under a sinusoidal Hs. (B) The variation of l over time under the sinusoidal Hs. (C) Schematic illustration and experimental microscopic images of the motions of the microengine in one period (a−f), representing the guiding effect of the DTPs with a time-varying l (a−f in B) under the sinusoidal Hs. Scale bars, 10 μm.

the microengine moves near the substrate wall, the microengine can be guided to hit the wall and trapped (Figure 5C and Video S8), further verifying the guided motion in z direction. The results shown in Figures 4 and 5 suggest that the DTPs can guide microengines in three-dimension, and the orientation of the microengines with respect to z axis can be reflected through their structural colors. In the as-demonstrated DTP guidance strategy, microengines are simply guided to move in various complex trajectories, such as semi-sine and sinusoidal trajectories by a time-varying H. As shown in Figure 6A and Video S9, when a sinusoidal field Hs = H0 sin(2πft) is applied by Helmholtz coils (Figure S8), in which H0 (92 Gs) is the amplitude of the applied sinusoidal field and f (3 Hz) is the frequency, the microengine moves in a semi-sine trajectory. This complex trajectory can be attributed to the guiding effect of the DTPs with a time-varying l (Video S10). As shown in Figures 6B and S9A, l varies periodically with a frequency of 6 Hz following l = l0|sin(2πf t)|, in which l0 is 26.3 μm. Figure 6C demonstrates

As the DTPs consist of periodically assembled monodispersed Fe3O4@PVP nanoparticles,42 they show bright structural colors when their tilting angle (θ) relative to z axis is within 45° (Figure 5A) according to Bragg’s law,53−55 in which the diffraction wavelength: λ = n(δ1 + δ2) = nd[cos(φ − θ ) + cos θ )]

(3)

where n is the effective refractive index, δ = δ1 + δ2 is the optical path difference, and d is the lattice spacing corresponding to the distances between two neighboring nanoparticles. In our experimental setup, the angle between the incident light and back scattered light (φ) is 29°. Figure 5B and Video S8 indicate that when DTPs are tilted with a decreasing θ from 90 to 0° under H, the color of DTPs gradually changes from native brown color to blue and green (Figure S7), and the microengine gradually dives and disappears from the focal plane due to its motion in z direction. When H is off and the DTPs are dissembled, the microengine may rise to the focal plane again (Video S8). If E

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Figure 7. (A) Schematic illustration and experimental microscopic images depicting the guidance of the microengine by DTPs in one period under the oscillating He ( f = 2 Hz). Scale bar, 20 μm. (B) The variation of Hy (Hy = H0 sin(2πf t)) over time in one period, and the corresponding microengine displacement in y axis over time, which follows an equation of y = y0 sin(2πf t − π/2). Points a−d in the curves correspond to the position of the microengine at 0, 0.14, 0.4, and 0.5 s in (A). (C) Optical microscopic images and motion trajectories (red curves) of a microengine under an oscillating He with different f. Scale bar, 20 μm. (D) The dependence of y0 on f of Hy, suggesting that y0 decreases with the increasing f. He was applied by Helmholtz coils.

2), in which y0 (18.9 μm) is the amplitude of the sinusoidal trajectory. As the microengine would move uphill with an increasing y from −y0 to y0 as long as Hy is positive, and goes downhill if Hy is negative, thus there is an offset of π/2 between y and Hy, as shown in Figure 7B. Points a−d in these curves correspond to positions of the microengine at 0, 0.14, 0.4, and 0.5 s in Figure 7A. Furthermore, from the trajectory equation, the trajectory of the microengine can be easily controlled by adjusting f of the applied Hy. As shown in Figure 7C and Video S11, the frequency of the microengine trajectory can be controlled to be 2, 4, 6, and 8 Hz by following f of the oscillating DTPs under He. Meanwhile, the amplitude y0 decreases gradually (Figure 7D) because there is less time for the microengine to move in y axis with increasing f. Steering living cells is of significance for their applications in drug delivery, sensing, micro/nanoengineering, and environmental remediation.56,57 To achieve magnetic controllability, living cells usually need to be artificially magnetized by embedding magnetic nanoparticles or attaching them to magnetic substrates.56 However, the artificial magnetization requires complex processing steps and inevitably changes cell behaviors or even affects cell viability. The as-proposed DTPs can steer living cells (a green alga is shown as an example here) without the requirement of the artificial magnetization. As

the schematic illustration and experimental microscopic images of the moving microengine in one period (a−f) under the navigation of DTPs when the sinusoidal Hs is applied. In the first half period, with l gradually increases from 0 to l0 (a−c in Figure 6C), the moving microengine gradually turns its longitude axis aligned to the DTPs, as depicted the rotation of red arrows in Figure 6C. In the second half period, with l gradually decreases from l0 to 0 (d−f in Figure 6C), the aligned microengine gradually rotates its longitude axis back to the origin orientation when moving. As a result, a semi-sine trajectory is resulted, and both l and the motion trajectories show steadily periodic variations over time. By applying a time-varying magnetic field He oscillating around x axis, which includes a homogeneous static field Hx (66 Gs) in x axis and a sinusoidal field Hy = H0 sin(2πf t) with controlled f in the direction perpendicular to Hx, DTPs successively oscillate around x axis (Figure S9B and Video S10) to follow He. Due to the guiding effect of DTPs, the microengine changes its motion direction successively along the oscillating DTPs and thus shows a sinusoidal trajectory (Video S11). Figure 7A shows the schematic diagrams and microscopic images depicting motions of the microengine in one period under the oscillating He with an f of 2 Hz. The sinusoidal trajectory follows an equation y = y0 sin(2πf x − π/ F

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Figure 8. Optical microscopic images and trajectories (green and red curves) of a green alga (A, C) without and (B) with the guidance of DTPs when H (100 Gs, applied by a permanent NdFeB magnet) is off and on, respectively. Scale bar, 20 μm.

responses of micromotors and apply to autonomously propelling agents swimming both in bulk and near substrate walls. Furthermore, the as-developed integrated aqueous system consisting of magnetic nanoparticles and microengines (or motile microorganisms) may inspire the development of intelligent integrated systems with cooperative functions for biomedical and environmental applications.

shown in Figure 8 and Video S12, due to the isotropic and biocompatible environment, the green alga moves freely and exhibits a random walk (Figure 8A) in the ferrofluid with Cp of 60 mg/mL without H. The green alga continues to move in a curved trajectory for about 1 s after H (100 Gs) is on until DTPs reach to its l* (31 μm at 3 s). Then, the green alga moves along the DTPs nearly in a straight-line trajectory (Figure 8B). It is also found that the green alga jumps the rails (4.6−5 s in Figure 8B) more easily than the tubular microengine when it meets a gap because of its spherical shape and vigorous random walks. Once DTPs disassemble when H is off, the green alga moves freely again (Figure 8C). These results suggest that DTPs not only can guide artificial microengines but also worked to steer motile living cells without the requirement of harmful and complex processing steps. Recently, to guide micro/nanomotors directly obviating the reliance on their customized responses, various topographical pathways have been developed by utilizing local boundaries or obstacles to control the motor alignment, local product distribution, flow fields, etc.33−37 However, these topographical pathways are rigid and required to be sculptured on the substrates in advance. Thus, they suffer from poor flexibility and are not applicable for the guidance of micro/nanomotors swimming in bulk. In contrast, the DTPs in ferrofluids can suspend in bulk and are controllable in the formation, length and directions, offering a high flexibility in the guidance of artificial microengines and motile microorganisms (Figures 3−8). Furthermore, as separated functional materials, magnetic nanoparticles are promising in biomedical and environmental applications, including drug delivery, magnetic resonance imaging, hyperthermia, toxin removal, etc.,44−46 and microengines can perform various tasks, such as sensing, cargo transport, microsurgery, etc.10,43,58 Hence, the coexistence of functional magnetic nanoparticles and microengines in a liquid medium may create an integrated multifunctional system for various applications.

EXPERIMENTAL SECTION Materials. All the chemicals used in this work were of analytical grade and were used as received without further purification. Poly(vinylpyrrolidone) (PVP, K30), D-(+)-glucose, ethylene glycol (EG), ferric chloride hexahydrate (FeCl3·6H2O), sodium acetate (NaAc), sodium cholate, hydrogen peroxide, KNO3, Triton X-100 (≥99%), methylene chloride (CH2Cl2), pyrrole (Py), chloroplatinic acid hexahydrate (H2PtCl6·6H2O), and ethanol were purchased from TCI Shanghai Chemical company, China. Cyclopore polycarbonate membranes containing 2 μm diameter conical-shaped micropores (catalog no. 7060−2511) were purchased from Whatman, Maidstone, U.K. Chlamydomonas reinhardtii strains 21gr (mt+) (CC-1690) were obtained from the Chlamydomonas Resource Center (University of Minnesota) and grown in liquid M medium at 23 °C with a 14/10 h light/dark cycle and constant aeration.59 Synthesis of Fe3O4@PVP NPs. The synthesis process is referenced from the previous work with some modifications.42 Briefly, PVP (K30, 45 mmol) and D-(+)-glucose (1.7 mmol) were added into EG (30 mL). The solution stirred for 10 min at 100 °C and cooled down to room temperature. Then, FeCl3·6H2O (2.5 mmol) was added into the solution and stirred for 30 min before NaAc (40 mmol) was added. The as-obtained solution was stirred for another 40 min and then transferred into a 50 mL Teflon-lined stainless-steel autoclave. The autoclave was sealed and maintained at 200 °C for 10 h. After being cooled to room temperature, the final product was collected by a magnet and rinsed with a mixture of ethanol and deionized water for several times. Synthesis of Catalytic Polypyrrole/Pt Tubular Microengines. The catalytic polypyrrole/Pt (PPy/Pt) tubular microengines were fabricated by a template-directed electrodeposition method. The template used in this process is a commercially available Cyclopore polycarbonate membrane, which contained 2 μm maximum diameter conical-shaped micropores. The polypyrrole (PPy) layers were electropolymerized at +0.806 V for a charge of 0.5 C from a plating solution containing 74 mM Py, 15 mM KNO3, and 1 wt % Triton X100, and the metallic Pt layers were deposited galvanostatically at −2 mA for 3000 s from a Pt solution containing 10 mM H2PtCl6·6H2O and 0.05 M HCl. To release the microengines, a gold layer, which was sputtered on one side of the porous membrane to serve as a working electrode, was completely removed by polishing with 5−6 μm alumina slurry. Then the membrane was dissolved in methylene chloride for 15 min to completely release the microengines. The microengines were collected by centrifugation and washed repeatedly with methylene chloride, ethanol, and ultrapure water. All microengines were stored in ultrapure water at room temperature. Guidance of Nonmagnetic Microengines in Ferrofluids. The prepared microengines were dispersed in 100 μL aqueous ferrofluid with Fe3O4@PVP NPs, hydrogen peroxide (7% v/v), and sodium

CONCLUSIONS In conclusion, we have demonstrated a flexible guidance of nonmagnetic microengines in ferrofluids by dynamic topographical pathways (DTPs). In this flexible guidance strategy, the DTPs with controlled lengths and directions can be reversibly assembled by superparamagnetic Fe3O4@PVP NPs in the ferrofluid in response to external magnetic fields. They can regulate the orientation and motion directions of moving microengines through exerting anisotropic resistance forces on them in real time and thus generate various trajectories from circular, elliptical, straight-line, semi-sine, to sinusoidal ones. The as-demonstrated simple, versatile, and real-time motion guidance strategy may obviate reliance on the customized G

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ACS Nano cholate (0.5 wt %). The microengines exhibited autonomous bubblepropelled motions in the ferrofluid when no magnetic field (H) is applied. Helmholtz coils powered by a DC (DX3005DS, Daxin, China) and/or an AC power source (APS-1102A, GWINSTEC, China) and a permanent NdFeB magnet were used to generate homogeneous, time-varying, and gradient H to control formation, length, and the direction of DTPs. The intensity of H was measured by a Gauss meter and controlled by adjusting the current of the DC and AC power sources, or the distance between the permanent NdFeB magnet and the sample. The average length of DTPs at different conditions and its standard deviation were calculated from the lengths of over 50 DTPs. The guidance of green algae by the DTPs was also conducted according to above protocols. All videos were recorded at room temperature by using an inverted optical microscope (Leica DMI 3000 M), coupled with 10, 20, and 50 objectives. All videos were analyzed by Video Spot Tracker V08.01 software.

Funds for the Central Universities (WUT: 2017III028, 2018III012, 2016III009, and 2015III060). We also acknowledge Prof. Zhangfeng Hu (Jianghan University, Wuhan) for providing green algae.

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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/acsnano.8b01682. Scanning electron microscopy (SEM) images of the PPy/Pt tubular microengine and Fe3O4@PVP NPs, motion trajectories of the microengines in the medium without DTPs, the average length (l) of DTPs at different time and Cp, optical microscopic images depicting the interactions between microengines and DTPs, the diffractive color changes of DTPs with different θ, and the changes of DTP length and direction under time-varying magnetic field Hs and He, the change of magnetic intensity of Hs over time, and description of 12 supporting videos (PDF) Video S1 (AVI) Video S2 (AVI) Video S3 (AVI) Video S4 (AVI) Video S5 (AVI) Video S6 (AVI) Video S7 (AVI) Video S8 (AVI) Video S9 (AVI) Video S10 (AVI) Video S11 (AVI) Video S12 (AVI)

AUTHOR INFORMATION Corresponding Authors

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

Fangzhi Mou: 0000-0002-9644-8277 Jianguo Guan: 0000-0002-2223-4524 Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation of China (21474078, 51303144, 21705123, 51573144, 51303143, and 51521001), the Top Talents Lead Cultivation Project and Natural Science Foundation of Hubei Province (2015CFA003), the Yellow Crane talents plan of Wuhan municipal government, and the Fundamental Research H

DOI: 10.1021/acsnano.8b01682 ACS Nano XXXX, XXX, XXX−XXX

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DOI: 10.1021/acsnano.8b01682 ACS Nano XXXX, XXX, XXX−XXX