Magnetic Active Matter Based on Helical Propulsion - Accounts of

Article Cite This: Acc. Chem. Res. XXXX, XXX, XXX−XXX

pubs.acs.org/accounts

Magnetic Active Matter Based on Helical Propulsion Published as part of the Accounts of Chemical Research special issue “Fundamental Aspects of Self-Powered Nano- and Micromotors”. Pranay Mandal,† Gouri Patil,‡ Hreedish Kakoty,‡ and Ambarish Ghosh*,†,‡ †

Centre for Nano Science and Engineering, Indian Institute of Science, Bangalore 560 012, India Department of Physics, Indian Institute of Science, Bangalore 560 012, India

‡

Acc. Chem. Res. Downloaded from pubs.acs.org by REGIS UNIV on 10/23/18. For personal use only.

S Supporting Information *

CONSPECTUS: Micro- and nanomotors are nonliving micro- and nanoparticles that are rendered motile by supplying energy from external sources, for example, through asymmetric chemical reactions or the application of electric, magnetic, optical, or acoustic fields. Their study is interesting for two reasons. First, nanomotors can impact future biomedical practices, where one envisions intelligent multifunctional nanomachines swarming toward a diseased site and delivering therapeutics with high accuracy. The second motivation stems from the prevalence of self-powered systems in nature, ranging from intracellular transport to human migration, which are nonequilibrium phenomena yet to be completely understood. Nanomotors provide a promising route toward the study of complex active matter phenomena with a welldefined and possibly reduced set of variables. Among different ways of powering nanomotors, magnetic field deserves a special mention because of its inherent biocompatibility, minimal dependence on properties of the surrounding medium, and remote powering mechanism. In particular, magnetically actuated propellers (MAPs), which are helical structures driven by rotating fields in fluids and gels, have been demonstrated to be highly suitable for various microfluidic and biotechnology applications. Unfortunately, this method of actuation requires direct application of mechanical torque by the applied field, implying that the system is driven and therefore cannot be considered self-propelled. To overcome this fundamental limitation, we discuss an alternate magnetic drive where the MAPs are powered by oscillating (not rotating) magnetic fields. This technique induces motility in the form of back-and-forth motion but allows the directionality to be unspecified, and therefore, it represents a zero-force, zero-torque active matter where the nanomotors behave effectively as selfpropelled entities. The MAPs show enhanced diffusivity compared with their passive counterparts, and their motility can be tuned by altering the external magnetic drive, which establishes the suitability of the MAPs as model active particles. Enhancement of the diffusivity depends on the thermal noise as well as the inherent asymmetries of the individual motors, which could be well-understood through numerical simulations. In the presence of small direct-current fields and interactions with the surface, the swimmers can be maneuvered and subsequently positioned in an independent manner. Next, we discuss experimental results pertaining to the collective dynamics of these helical magnetic nanoswimmers. We have studied nonmagnetic tracer beads suspended in a medium containing many swimmers and found the diffusivity of the beads to increase under magnetic actuation, akin to measurements performed in dense bacterial suspensions. In summary, we envision that rendering the system of MAPs active will not only provide a new model system to investigate fundamental nonequilibrium phenomena but also play a vital role in the development of intelligent theranostic probes for futuristic biomedical applications. bacterial suspension,12 which depends on a complex interplay13 of confinement,14 activity,10 steric and hydrodynamic interactions,15 proximity to a surface,16 etc.; many of these dependencies have been mimicked in nanomotor-based systems. For example, the strong relationship of active matter phases17 to the density18 and shape19 of the individual constituents and their unusual rheological properties,20 fluctuations,21 and dependence on the surrounding environment22 are well-established. It is also noteworthy that natural active systems are usually

1. INTRODUCTION The richness of active matter phenomena1−3 is not limited to the natural world, and in fact, many emergent phenomena such as flocking and swarming of birds/insects and predator−prey behavior can be mimicked in artificial systems, where motility is induced externally at the scale of individual particles. Initial efforts4,5 were primarily based on powering by asymmetric chemical reactions, followed by other techniques such as electric,6 magnetic,7 optical,8 and acoustic fields9 in both wet and dry10,11 environments. The advantages of “nanomotors”2,3 arise from their simplicity, where experimental variables are fewer in number and easier to control. A familiar example is the state of a © XXXX American Chemical Society

Received: June 29, 2018

A

DOI: 10.1021/acs.accounts.8b00315 Acc. Chem. Res. XXXX, XXX, XXX−XXX

Article

Accounts of Chemical Research

Figure 1. (a) Quincke rotation and self-propulsion of a colloidal roller. (b) Vortex of rollers (black, position; blue, speed). (c) Schematic of ICEP. (d, e) Chains and clusters of Janus spheres formed due to ICEP. (f) Au−silica Janus bead under defocused laser illumination. (g, h) Trajectories of the beads with/without illumination. (i) Hematite cube (arrow) along with colloidal tracers and accumulation of tracers on the hematite cube surface under blue laser illumination. (j) Particles from different clusters (false-colored) forming new clusters. (k) Schematic of acoustic propulsion of metallic rods. (l) Acoustic propulsion inside a HeLa cell. (m) SEM image of a magnetic nanopropeller. (n) Controlled actuation of a magnetic helix inside a HeLa cell. Reproduced with permission from (a) ref 15, copyright 2013 Springer; (b) ref 33, copyright 2015 Springer; (c) ref 6, copyright 2008 American Physical Society; (d, e) ref 34, copyright 2016 Springer; (f−h) ref 8, copyright 2010 American Physical Society; (i, j) ref 35, copyright 2013 AAAS; (k) ref 9, copyright 2012 American Chemical Society; (l) ref 36, copyright 2014 Wiley; (m) ref 7, copyright 2009 American Chemical Society; (n) ref 37, copyright 2018 Wiley.

studied in their steady states, while artificial systems can be used to study kinetic phenomena.23 Apart from acting as model systems for the study of nonequilibrium phenomena, nanomotors have strong technological potential. The central aim24 is to develop nanovehicles that can be driven in vivo to carry out various biomedical applications. The toxicity and biocompatibility requirements exclude nanomotors4,5 that are powered by toxic chemicals like H2O2, although there are efforts to develop inherently biocompatible enzyme-based25 and cell-based motors.26,27 An alternate strategy is to induce motility using nonchemical forces, especially using magnetic fields.24,28 Interesting ideas can be borrowed from active matter phenomena, e.g., schooling29 and migration,30 to impart collective intelligence,31 thereby achieving better targeting efficiency.32 While this virtual special issue of the journal focuses on selfpropelled chemical motors, the focus of this Account is to highlight and discuss motors that are powered through nonchemical means. The motivation and crucial differences

are the following: (i) Chemical motors depend strongly on properties of the nanomotor surface and surrounding medium, which is not generally true for motors driven by physical fields. (ii) The reaction conditions change with time because of fuel depletion in chemically powered systems; microfluidic flow devices may help in this regard but can become cumbersome because of the formation of bubbles at high motor activities/ densities. (iii) Motility in chemically powered motors is typically induced through phoretic transport or formation of bubbles in an asymmetric structure. On the other hand, physical fields induce motility through generation of local phoretic gradients by external power sources or through direct transduction of mechanical motion by an external force/torque. Here we briefly mention (Figure 1) a few nonchemical routes to induce motility, with a detailed discussion of magnetically actuated propellers (MAPs). Although well-suited for microfluidic and biomedical applications, MAPs are not self-propelled under rotating fields. Through a subtle modification of the magnetic drive, it is possible to induce motility in the system B


Article


of micro- and nanoscale magnetized helices, including flexible44 and biomaterial-based structures,45,46 are available.

by applying a net zero external force and torque, as in model self-propelled entities1 such as living microorganisms and chemical nanomotors. The swimmers described here experience an externally applied instantaneous torque that vanishes for single motors when time-averaged. Also, the swimmers are randomly oriented in the absence of interactions, implying that the ensemble-averaged instantaneous external torque/force is zero. Thermal fluctuations and small direct-current (dc) magnetic fields can affect their motility, and multiple MAPs, through surface interactions, can be positioned independently. We will discuss the challenges to scale up this novel active matter to higher densities and activities and show preliminary results on their collective dynamics.

Dynamics and Fluctuations

The past decade has seen considerable interest in obtaining fundamental understanding and demonstrating applications with MAPs. In general, rotating magnetic fields are applied to ferromagnetic helices, which cause the helices to rotate and therefore translate along the direction governed by the sense of rotation of the fields and the handedness47 of the helices. The speed of each helix increases linearly with frequency until the viscous drag experienced by the helix balances the available torque. Beyond this so-called “step-out frequency”, the MAP cannot rotate synchronously with the field and hence moves slower. The viscous drag and therefore the dynamics of the MAPs are sensitive to nearby solid surfaces, which can occur when they sediment close to the bottom of the fluidic chamber. As the helix dimensions are reduced, orientational diffusion becomes dominant,48 which puts a practical limit of approximately 1 μm on the length of MAPs in a Newtonian fluid like water (viscosity ≈ 1 cP). Related studies of the optimal shape49 and length of the MAP suggest that about one full turn maximizes the hydrodynamic pitch.50 Deviation from this simple picture occurs when the MAPs are driven in complex media, such as suspensions51 or gel-like networks.52,53 The application of a rotating field shows dynamics other than propulsion, e.g., a precessing/wobbling54 motion when the magnetization is at an arbitrary angle to the helical axis. This was understood55 by considering the rigid-body dynamics of an elongated structure under an external torque at low Reynolds numbers, which formed the basis of a microfluidic viscometer53 where the nanomotor moves through and maps the local rheological properties of a complex fluid. Stability analysis suggests that close the step-out frequency, multiple stable dynamical configurations exist. This was experimentally54 confirmed when arbitrarily magnetized MAPs switched randomly between tumbling and propelling states.

2. NANOMOTORS POWERED BY PHYSICAL METHODS We limit our discussion to nanomotors driven in wet systems by nonchemical methods. In certain cases, the external field causes phoretic flow around the nanomotor. For example, Au− SiO2 particles under illumination have localized heat gradients, resulting in enhanced diffusivity8 via thermophoresis. Other examples with light include the motion of AgCl particles29 and TiO2 micromotors38 under UV illumination due to diffusiophoresis induced by photocatalytic activity. Recently Palacci et al.35 showed that dynamic assemblies of photoactivated colloids form through a balance between self-propulsion and attractive interactions. Electric fields can induce phoretic drive, e.g., by differential ionic flows on two sides of Janus spheres, which move perpendicular to an applied alternating-current electric field through induced-charge electrophoresis (ICEP).6 A subtle modification led Yan et al.34 to see collective behavior in this system. Alternatively, in Quincke rotation, the charge distribution on insulating spheres in conducting fluids leads to instabilities beyond a critical electric field, where the spheres rotate and move transverse to the field direction,15 and collective behavior of the same were reported by Bricard et al.33 Another approach for physical actuation is by ultrasonics,9 where colloidal rods were actuated inside living cells36 through self-acoustophoresis.

Biological Applications

Controlled manipulation of MAPs in biologically relevant ex vivo environments such as living cells,37 human blood,51 urine,44 and mucine gel56 and in vivo environments such as the peritoneal cavity of mice57 has been demonstrated. Certainly, for biomedical applications we need to maneuver many nanomotors simultaneously; however, at high densities, the suspension containing the helices can lose stability as a result of magnetic agglomeration. To circumvent this issue, superparamagnetic helices,58 which do not agglomerate in the absence of a field, have been used. Alternately, a spacer layer59 around the ferromagnetic helices can reduce the agglomeration. The layer is multifunctional: it protects the magnetic element from chemical corrosion51 and has high magnetic hyperthermia59 potential to target cancer cells selectively.

Magnetically Driven Helical Nanomotors

Driving colloids with spatially homogeneous magnetic fields requires special strategies, since permanent or induced magnetic dipoles can align to an external field but cannot move like an isolated charge drifting under the action of a homogeneous electric field. At small scales, motion in fluids is dominated by viscosity, which requires special swimming techniques.39 Commonly used strategies are based on mimicking the motion of microorganisms, such as the beating motion of a cilia or corkscrew motion of bacterial flagella. Although microorganisms are intrinsically self-propelled, artificial cilia or helical flagella are made motile (magnetically) through direct conversion of mechanical energy by applied magnetic fields, implying that they are under a finite external force/torque. Recent advances in nanofabrication have contributed to development of novel magnetic colloids40,41 with a high degree of geometrical and functional complexity. Magnetically induced beating motion of artificial cilia-like structures was achieved with interconnected magnetic colloids.42 Corkscrew motion was mimicked with artificial helical magnetic structures with lengths of 40 and 2 μm that were fabricated using the selfscrolling technique43 and glancing-angle deposition (GLAD),7 respectively. Currently, various demonstrations of the fabrication

Multifunctionality

To summarize, MAPs are promising candidates for technological applications pertaining to biomedicine and microfluidics. Some of their advantages translate directly to the constitution of novel artificial active matter, since the motility of the nanomotors can be engineered and controlled through external magnetic fields in variety of media. Versatile fabrication strategies allow the integration of multiple functions within a single nanomotor, providing additional interesting C


Article


Figure 2. Magnetic actuation by rotating and oscillating fields. (a) Schematic and SEM image of a helical nanomotor. The red arrow shows the direction of the permanent magnetization due to a thin cobalt film. Also shown schematically is the propulsion of many motors under a rotating magnetic field, where all the helices move in the same direction. (b) Random orientations of the helical microstructures in the xy plane when the applied field is only along the z direction. The magnetic moments are pointed in random directions when Bz = 0 and along the +z or −z direction depending on the direction of Bz. (c) Rotation of the helices for an oscillating magnetic field along the ±z axis. The sense of rotation can be either clockwise or counterclockwise, accompanied by forward or backward translation, depending on the handedness of the helix. The schematic is viewed approximately along the long axis of the motor. (d) Schematic of the orientation of the helix in the xy plane (same as the imaging plane), which is randomized by thermal noise. (e) Collection of helices under an oscillating field, which are motile along different directions.

turn clockwise (CW) or counterclockwise (CCW) to keep the moment parallel to the applied field, which depending on the handedness of the helix can result in a forward or backward p displacement of ± 2h , where ph is the hydrodynamic pitch of the helix. Crucially the orientation of an individual helix remains unspecified and randomized because of thermal fluctuations, as shown in Figure 2d. Clearly, the energy input by the oscillating field can induce motility without any control over directionality. This ensures that the time-averaged external torque will be zero, as is the case for all self-propelled particles. In the absence of any aligning interactions, a collection of such MAPs would move along independent directions (Figure 2e). As shown in Figure 2c, the rotation about the long axis of the helix is predicted to be either CW or CCW with equal probability. This contrasts with the experimental results, where we observed the helices to execute an almost perfect sequence of CW and CCW rotations. One such sequence is shown in the inset of Figure 3a, where all of the events except for the fifth and 14th follow a perfect sequence of alternating CW and CCW turnings. The reciprocal event sequence could be explained by the asymmetry in the weight distribution of the helix, primarily due to the thin magnetic coating on one side of the helix. As explained in Figure 3b, when the magnetic field flips its direction from the +z axis to the −z axis, the torque due to the weight asymmetry makes the helix undergo a CW rotation along its long axis and vice versa. To further confirm the proposed mechanism, the dynamics of the helix was modeled as

handles. For example, plasmonic nanoparticles can be integrated with MAPs, allowing the motors to work as mobile nanotweezers60 under optical illumination. This technique allows the pickup, transport, delivery, and on-chip assembly of submicron cargoes, including fluorescent nanodiamonds and living bacteria, that are not possible otherwise. Illumination can generate local heat and therefore thermophoretic flows close to the nanomotor, allowing phoretic effects to be integrated into the same motor. It will be interesting to study the behavior of a collection of multifunctional MAPs.

3. FROM DRIVEN TO SELF-PROPELLED ACTIVE MATTER MAPs driven by rotating fields are not active in the same sense as self-propelled living microorganisms or catalytic nanomotors. The rotating field applies a torque, which results in parallel manipulation of a collection of motors, as shown in Figure 2a. The MAPs were fabricated by GLAD61 with a thin magnetic coating on one side of the helix. A microfluidic chamber containing helices dispersed in deionized water was placed at the focal plane of the microscope objective. We observed the motors to move parallel to each other under a rotating drive. This was clearly different from the motion of self-propelled colloids, whose directions are governed by orientational diffusion and/or interactions with other active constituents. To decouple their motility and directionality, we consider an oscillating62 magnetic field along the z direction. As shown in Figure 2b, the magnetic moment remains aligned with Bz and becomes random when Bz = 0; however, the orientation of the helices always remains unspecified and subject to thermal randomization. We show a schematic representation of the motion of the helices driven by Bz in Figure 2c. The helix can

−mBz (t ) sin(α) + WR sin(α + ϕ) = γl

dα dt

(1)

where R is the radius of the helix, γl is the rotational drag coefficient of the helix about the long axis, and m and W are D


Article


Figure 3. (a) Mechanism of reciprocal swimming as seen along the helical long axis, where α is the angle between the direction of the magnetization and the z axis. Misalignment of this direction and the line of action of the weight causes the helix to rotate CW (CCW) when the field changes from +z to −z (−z to +z). The inset shows a sequence of turning as observed experimentally, with arrows showing events where the CW−CCW reciprocity symmetry is broken. (b) Temporal evolution of α as seen in the simulation. Upper panel: Alternating sequence of CW and CCW rotation in the absence of thermal noise. The time of rotation, ∼10 ms, is close to the experimentally measured value (∼13 ms). Lower panel: In the presence of thermal fluctuations, the perfectly reciprocal turning sequence is broken (circled), shown here as CCW−CCW−CW− CCW−CW−CCW−CCW. Reproduced with permission from ref 62. Copyright 2013 American Physical Society.

the magnetic moment and weight of the magnetic film, respectively. The time dependence of the rotational angle dα (upper panel of Figure 3b), given by α(t+Δt) = α(t) + dt Δt , where Δt is the time step of the simulation, shows reciprocal turning, thus validating the proposed mechanism. When thermal fluctuations are incorporated into the model (lower panel of Figure 3b), certain rotations that break a perfectly reciprocal sequence can be seen, similar to what was observed in the experiments. As discussed by Purcell,39 barring a few exceptions,63 backand-forth motion of swimmers cannot produce net displacement (the “scallop theorem”). However, in the presence of thermal noise, orientational diffusion of the helices leads to net displacement, even for a single cycle of back-and-forth motion. This gives rise to enhanced diffusivity64 of the reciprocal swimmers compared with their passive counterparts. A comparison between trajectories of Brownian and actuated helices is shown in Figure 4a. The corresponding mean-square displacement (MSD) plot, shown in Figure 4b, provides the enhancement in diffusivity (ΔD), given by

ΔD = ph 2 fB tanh

1 /8 4fB τr

(2)

where f B is the frequency of the oscillating field and τr is the Brownian orientational time scale of rotation about the short axis of the helix. The analytic expression given in eq 2, corresponding to a perfectly reciprocal sequence, predicts an enhancement of the diffusivity that is significantly lower than what was experimentally measured. This was mainly due to occasional breakdown of the reciprocal sequence, as confirmed with numerical simulations. The model assumed a sequence of p pulses denoted by q1, q2, ..., where qi = + 2Th if i is even and rot

p

qi = − 2Th if i is odd, where Trot is the rotation time of the rot

helix under the oscillating field. The pulses represent translational speeds of the helix in a perfectly reciprocal sequence of CW and CCW turning events. To incorporate different levels of reciprocity (defined as q), certain turning events (e.g., the nth event) were reversed on the basis of a E


Article


Figure 4. Enhanced diffusion by reciprocal motion. (a) Comparison of experimentally obtained different trajectories (denoted by distinct colors) of a helix (left) without (Brownian) and (right) with actuation. (b) MSD as a function of time for Brownian (blue) and reciprocal (red) motion. The log−log plot (inset) shows oscillations in the MSD plot with a time period of 0.2 s, which corresponds to the magnetic actuation frequency (5 Hz). (c) Enhanced diffusion obtained from the analytic expression (eq 2) and simulation plotted as a function of actuating frequency for various levels (in percentage) of exception to the perfect reciprocal sequence. The symbols correspond to experimentally measured enhancements of diffusivity for helices with various levels of reciprocity in the turning sequence. Reproduced with permission from ref 62. Copyright 2013 American Physical Society.

sequence of uniformly distributed random numbers (0 < ri < 1) for rn > q. This strategy incorporated the different levels of reciprocity (q) in the numerical model to make a more realistic estimate of ΔD. Experimentally, the value of q was calculated as Q/N, where Q is the number of turns in the opposite direction to that of a perfectly reciprocal sequence with N events. In Figure 4c, the comparisons between the numerical and experimental results for ΔD for different levels of reciprocity are plotted as functions of the actuating frequency. Indeed, ΔD depends very strongly on q. The finite rotation time (Trot) of the helix was also included in the numerical simulations and found to be of lesser significance, as expected at low frequencies. Presence of a small (a few Gauss) dc magnetic field (Bxy ≈ 1−2 G) along any direction changed the results dramatically, giving rise to a back-and-forth rocking motion. This is explained in Figure 5a−c, where unlike the previous system, the reciprocal motion of the helix was largely influenced by the dc field. This occurred because the magnetic torque was higher than the torque generated by the body-weight asymmetry, even for constant fields as low as a few Gauss. Also, on average the helices were oriented along a direction determined by the strength of Bxy, the magnetic moment, and the frequency of actuation. Also important is the asymmetric shape of the MAPs, which occurred because they were fabricated on polystyrene beads. The helices were close to the bottom surface, so the two ends of the asymmetric helix experienced different drags, which caused the “rocking” motion to result in net motion. The drag asymmetry depended on whether the tail (without a bead; panel 1 in Figure 5c) or head (with a bead; panel 3 of Figure 5c) of the structure was closer to the bottom surface. A control

experiment (Figure 5d) further confirmed this picture, as the displacement of a nearly symmetric helix (with the polystyrene bead etched) was significantly reduced compared with an asymmetric helix under similar experimental conditions. On the basis of this idea, a method65 to independently position MAPs was developed. As shown in Figure 5e, by the use of a combination of an oscillating field (along lab z) and a dc field (in the lab xy plane), helices 1 and 2 were actuated along different directions (blue trajectories). Subsequently, a rotating field (red trajectories) was used to propel the MAPs in parallel. The outcome of such an overall actuation scheme was two helices positioned in an independent manner, with helix 2 positioned 30 μm from its initial location while the position of helix 1 remained unchanged. As argued,65 this strategy can be scaled up for many helices provided the that the number of actuation steps is proportionally increased. It should be noted, however, that the direction of each nanomotor in this magnetic field configuration is determined by the external drive, implying that they are not self-propelled like the MAPs doing reciprocal motion under oscillating fields. Oscillating magnetic fields have been applied to other nonhelical nanomotors as well, resulting in different types of dynamics. Microdimers66 made of magnetic Janus microspheres were shown to roll around each other and subsequently “walked” on the surface parallel to the oscillating field. Similarly, surface-assisted swarm motion of magnetic colloids using oscillating and rotating fields has been reported.67 Flexible magnetic nanomotors showed fishlike68 motion perpendicular to the direction of the oscillating field, applied along the plane of observation. Similar structures showed propulsion through “freestyle”69 strokes when the field was F


Article


Figure 5. Effects of Bxy, shape asymmetry, and the surface. (a) Schematic and (inset) photomicrograph of the helix orientation in the imaging plane for a dc field applied along the y direction. (b) Temporal evolution of the resultant field B due to constant Bxy and oscillating Bz field, which forms an arc in the yz plane that gives rise to a back-and-forth rocking motion. (c) Schematics of the “rocking” motion resulting in net displacement, where the reciprocity is broken due to the asymmetric interaction of the helix with the surface. Corresponding optical images are shown in the insets. (d) Helix trajectories upon actuation by an oscillating field in the presence of Bxy along the y direction. Inset: Trajectories of asymmetric and symmetric helices having similar strengths and directions of magnetization actuated over similar duration. The modulation in the displacement signifies back-and-forth motion of the microhelices. (e) Demonstration of independent positioning using two helices. Reproduced from ref 65. Copyright 2015 American Chemical Society.

the body, here at one end of the helix (Figure 6a; also see the supporting video). A schematic and a microscope image of a

oscillated perpendicular to the plane of observation; however, it showed directionality along the direction of a weak gradient field. It is natural to wonder whether the latter system would have motility but no directionality if the magnetic field gradient were removed.

4. TOWARD HIGHER ACTIVITY AND COLLECTIVE EFFECTS As shown in Figure 4c, the activity of the magnetic reciprocal swimmers can be tuned through actuation frequency f B. However, the presence of a small dc field in the xy plane, originating from nearby lab instrumentation such as the microscope, tends to keep the swimmer oriented along a certain direction (as discussed above in connection with Figure 5), unlike selfpropelled objects. This effect is enhanced at higher actuation frequencies, at which the time-averaged alignment of the magnetization to the applied field is maximized, as predicted by numerical simulations (unpublished). We recently measured Bxy with a high-sensitivity magnetic field sensor and subsequently canceled all of the stray fields in the experimental region. This allowed us to obtain higher f B and therefore achieve much higher activity with the magnetic reciprocal swimmers. This work will be reported in the near future. Indeed, it will be of great significance and interest if a collection of reciprocal swimmers can be studied to probe interesting phenomena, such as clustering, boundary aggregation, ordering phase transitions, etc. One challenge is to overcome the magnetic agglomeration, which can be reduced dramatically59 by incorporating the magnetic material within

Figure 6. Enhancement of tracer diffusivity in magnetic active matter. (a, b) Schematic of a collection of reciprocal swimmers with tracer particles, here polystyrene beads (blue, schematic). The change in fabrication is evident with the swimmers having the magnetic part embedded at one end. (c, d) Trajectories of tracer particles with (frequency 5 Hz) and without magnetic actuation, showing a clear increase of diffusivity in the actuated system.

collection of such reciprocal swimmers along with 1 μm tracer polystyrene particles are shown in Figure 6a,b, respectively. G


Article

Accounts of Chemical Research Biographies

We imaged the motion of the tracer particles with and without magnetic actuation and observed a clear increase in the tracer diffusivity under actuation, as shown in Figure 6c,d. These preliminary results studying the effect of active collective dynamics on diffusion of tracer particles can be compared with experiments by Wu and Libchaber70 with passive tracers in a bacterial bath. It will be interesting to find out whether the tracers placed in a collection of reciprocal swimmers will also show superdiffusive behavior at small times, and if so, how the exponents and time scales compare with those for the archetypal self-propelled (nonreciprocal) system studied before.

Pranay Mandal received his Ph.D. from the Centre for Nano Science and Engineering, Indian Institute of Science, Bangalore. Currently he is a postdoctoral fellow in the same department. His research interests include the study of magnetically actuated active and driven systems. Gouri Patil is pursuing her MS−Ph.D. in the Department of Physics at the Indian Institute of Science, Bangalore. She obtained her undergraduate degree in Physics from the University of Bangalore. Currently her focus is on the study of collective behavior of magnetic active matter. Hreedish Kakoty is a Ph.D. student in the Department of Physics at the Indian Institute of Science, Bangalore. He completed his undergraduate studies in Physics at the University of Delhi. His research focuses on the study of self-assembly of passive and active colloids under confinement.

5. CONCLUSION In this Account, we have discussed the development of nanomotors actuated by nonchemical routes, specifically helical swimmers powered by oscillating magnetic fields. An advantage of the nonchemical route is the possibility of tuning the activity of the system simply by changing the magnetic field and frequency; however, one must acknowledge that there are many experimental issues in realizing an all-magnetic active system. For example, large-scale fabrication of MAPs with a narrow range of magnetic and geometrical characteristics is not trivial; in addition, the experimental setup to actuate the swimmers is typically custom-built and complex. Nevertheless, many of these challenges have been met already, so the next step in the study of magnetic active matter will be centered around the investigation of collective phenomena and drawing parallels with known natural12 and artificial systems.15,29 The collective behavior is expected to be a strong function of the interswimmer interactions, which will be a strong function of the density and proximity to a surface. At very high densities, the role of magnetic interactions may not be negligible and therefore needs to be taken into account. An interesting longstanding challenge is to make the system nonreciprocal and to investigate the emergence of collective behavior. Preliminary results from our group suggest that engineering the field configuration and surface interactions may cause nonreciprocal turning behavior of the helical swimmers, opening many new possibilities. Finally, one must recognize the great technology potential available with the magnetic helical swimmers, especially for biomedical and microfluidic applications. It is natural to wonder how making the swimmers self-propelled can help these fantastic voyagers become more intelligent and effective in carrying out biomedical tasks, particularly in comparison with driven systems.

■

Ambarish Ghosh is currently the Prof. Ramakrishna Rao Chair Professor at the Centre for Nano Science and Engineering and an associate faculty member in the Department of Physics at the Indian Institute of Science, Bangalore. He received his undergraduate degree in Physics from IIT Kharagpur in India and his Ph.D. in Physics from Brown University in the USA. He received the Shanti Swarup Bhatnagar Prize in Physical Sciences in 2018. His scientific interests include plasmonics, quantum fluids, and active magnetic colloids and their applications in biotechnology.

■

ACKNOWLEDGMENTS We thank Dr. Haobijam Johnson Singh, Reshma V. R., and Souvik Ghosh for their help with fabrication and DBT and RGUHS for funding. We also acknowledge the funding from MHRD, MeitY, and DST Nano Mission for supporting the facilities at CeNSE.

■

(1) Ramaswamy, S. The mechanics and statistics of active matter. Annu. Rev. Condens. Matter Phys. 2010, 1, 323−345. (2) Elgeti, J.; Winkler, R. G.; Gompper, G. Physics of microswimmers-single particle motion and collective behavior: a review. Rep. Prog. Phys. 2015, 78, 056601. (3) Bechinger, C.; Di Leonardo, R.; Löwen, H.; Reichhardt, C.; Volpe, G.; Volpe, G. Active particles in complex and crowded environments. Rev. Mod. Phys. 2016, 88, 045006. (4) Paxton, W. F.; Kistler, K. C.; Olmeda, C. C.; Sen, A.; St. Angelo, S. K.; Cao, Y.; Mallouk, T. E.; Lammert, P. E.; Crespi, V. H. Catalytic nanomotors: autonomous movement of striped nanorods. J. Am. Chem. Soc. 2004, 126, 13424−13431. (5) Ozin, G. A.; Manners, I.; Fournier-Bidoz, S.; Arsenault, A. Dream nanomachines. Adv. Mater. 2005, 17, 3011−3018. (6) Gangwal, S.; Cayre, O. J.; Bazant, M. Z.; Velev, O. D. Inducedcharge electrophoresis of metallodielectric particles. Phys. Rev. Lett. 2008, 100, 058302. (7) Ghosh, A.; Fischer, P. Controlled propulsion of artificial magnetic nanostructured propellers. Nano Lett. 2009, 9, 2243−2245. (8) Jiang, H.-R.; Yoshinaga, N.; Sano, M. Active motion of a Janus particle by self-thermophoresis in a defocused laser beam. Phys. Rev. Lett. 2010, 105, 268302. (9) Wang, W.; Castro, L. A.; Hoyos, M.; Mallouk, T. E. Autonomous motion of metallic microrods propelled by ultrasound. ACS Nano 2012, 6, 6122−6132. (10) Melo, F.; Umbanhowar, P. B.; Swinney, H. L. Hexagons, kinks, and disorder in oscillated granular layers. Phys. Rev. Lett. 1995, 75, 3838. (11) Yamada, D.; Hondou, T.; Sano, M. Coherent dynamics of an asymmetric particle in a vertically vibrating bed. Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 2003, 67, 040301.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.accounts.8b00315.

■

REFERENCES

Video showing a collection of magnetic helical swimmers and passive particles under magnetic actuation (AVI)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Ambarish Ghosh: 0000-0002-2524-0014 Notes

The authors declare no competing financial interest. H


Article


(34) Yan, J.; Han, M.; Zhang, J.; Xu, C.; Luijten, E.; Granick, S. Reconfiguring active particles by electrostatic imbalance. Nat. Mater. 2016, 15, 1095. (35) Palacci, J.; Sacanna, S.; Steinberg, A. P.; Pine, D. J.; Chaikin, P. M. Living crystals of light-activated colloidal surfers. Science 2013, 339, 936−940. (36) Wang, W.; Li, S.; Mair, L.; Ahmed, S.; Huang, T. J.; Mallouk, T. E. Acoustic propulsion of nanorod motors inside living cells. Angew. Chem., Int. Ed. 2014, 53, 3201−3204. (37) Pal, M.; Somalwar, N.; Singh, A.; Bhat, R.; Eswarappa, S. M.; Saini, D. K.; Ghosh, A. Maneuverability of Magnetic Nanomotors Inside Living Cells. Adv. Mater. 2018, 30, 1800429. (38) Hong, Y.; Diaz, M.; Córdova-Figueroa, U. M.; Sen, A. LightDriven Titanium-Dioxide-Based Reversible Microfireworks and Micromotor/Micropump Systems. Adv. Funct. Mater. 2010, 20, 1568−1576. (39) Purcell, E. M. Life at low Reynolds number. Am. J. Phys. 1977, 45, 3−11. (40) Tierno, P.; Golestanian, R.; Pagonabarraga, I.; Sagués, F. Controlled swimming in confined fluids of magnetically actuated colloidal rotors. Phys. Rev. Lett. 2008, 101, 218304. (41) Driscoll, M.; Delmotte, B.; Youssef, M.; Sacanna, S.; Donev, A.; Chaikin, P. Unstable fronts and motile structures formed by microrollers. Nat. Phys. 2017, 13, 375. (42) Dreyfus, R.; Baudry, J.; Roper, M. L.; Fermigier, M.; Stone, H. A.; Bibette, J. Microscopic artificial swimmers. Nature 2005, 437, 862. (43) Zhang, L.; Abbott, J. J.; Dong, L.; Kratochvil, B. E.; Bell, D.; Nelson, B. J. Artificial bacterial flagella: Fabrication and magnetic control. Appl. Phys. Lett. 2009, 94, 064107. (44) Gao, W.; Sattayasamitsathit, S.; Manesh, K. M.; Weihs, D.; Wang, J. Magnetically powered flexible metal nanowire motors. J. Am. Chem. Soc. 2010, 132, 14403−14405. (45) Gao, W.; Feng, X.; Pei, A.; Kane, C. R.; Tam, R.; Hennessy, C.; Wang, J. Bioinspired helical microswimmers based on vascular plants. Nano Lett. 2014, 14, 305−310. (46) Steager, E.; Kim, C.-B.; Patel, J.; Bith, S.; Naik, C.; Reber, L.; Kim, M. J. Control of microfabricated structures powered by flagellated bacteria using phototaxis. Appl. Phys. Lett. 2007, 90, 263901. (47) Schamel, D.; Pfeifer, M.; Gibbs, J. G.; Miksch, B.; Mark, A. G.; Fischer, P. Chiral colloidal molecules and observation of the propeller effect. J. Am. Chem. Soc. 2013, 135, 12353−12359. (48) Ghosh, A.; Paria, D.; Rangarajan, G.; Ghosh, A. Velocity fluctuations in helical propulsion: how small can a propeller Be. J. Phys. Chem. Lett. 2014, 5, 62−68. (49) Keaveny, E. E.; Walker, S. W.; Shelley, M. J. Optimization of chiral structures for microscale propulsion. Nano Lett. 2013, 13, 531− 537. (50) Walker, D.; Kubler, M.; Morozov, K.; Fischer, P.; Leshansky, A. Optimal length of low reynolds number nanopropellers. Nano Lett. 2015, 15, 4412−4416. (51) Venugopalan, P. L.; Sai, R.; Chandorkar, Y.; Basu, B.; Shivashankar, S.; Ghosh, A. Conformal cytocompatible ferrite coatings facilitate the realization of a nanovoyager in human blood. Nano Lett. 2014, 14, 1968−1975. (52) Schamel, D.; Mark, A. G.; Gibbs, J. G.; Miksch, C.; Morozov, K. I.; Leshansky, A. M.; Fischer, P. Nanopropellers and their actuation in complex viscoelastic media. ACS Nano 2014, 8, 8794−8801. (53) Ghosh, A.; Dasgupta, D.; Pal, M.; Morozov, K. I.; Leshansky, A. M.; Ghosh, A. Helical Nanomachines as Mobile Viscometers. Adv. Funct. Mater. 2018, 28, 1705687. (54) Ghosh, A.; Paria, D.; Singh, H. J.; Venugopalan, P. L.; Ghosh, A. Dynamical configurations and bistability of helical nanostructures under external torque. Phys. Rev. E 2012, 86, 031401. (55) Ghosh, A.; Mandal, P.; Karmakar, S.; Ghosh, A. Analytical theory and stability analysis of an elongated nanoscale object under external torque. Phys. Chem. Chem. Phys. 2013, 15, 10817−10823.

(12) Budrene, E. O.; Berg, H. C. Dynamics of formation of symmetrical patterns by chemotactic bacteria. Nature 1995, 376, 49. (13) Wioland, H.; Woodhouse, F. G.; Dunkel, J.; Kessler, J. O.; Goldstein, R. E. Confinement stabilizes a bacterial suspension into a spiral vortex. Phys. Rev. Lett. 2013, 110, 268102. (14) Das, S.; Garg, A.; Campbell, A. I.; Howse, J.; Sen, A.; Velegol, D.; Golestanian, R.; Ebbens, S. J. Boundaries can steer active Janus spheres. Nat. Commun. 2015, 6, 8999. (15) Bricard, A.; Caussin, J.-B.; Desreumaux, N.; Dauchot, O.; Bartolo, D. Emergence of macroscopic directed motion in populations of motile colloids. Nature 2013, 503, 95. (16) Kümmel, F.; ten Hagen, B.; Wittkowski, R.; Buttinoni, I.; Eichhorn, R.; Volpe, G.; Löwen, H.; Bechinger, C. Circular motion of asymmetric self-propelling particles. Phys. Rev. Lett. 2013, 110, 198302. (17) Vicsek, T.; Czirók, A.; Ben-Jacob, E.; Cohen, I.; Shochet, O. Novel type of phase transition in a system of self-driven particles. Phys. Rev. Lett. 1995, 75, 1226. (18) Buttinoni, I.; Bialké, J.; Kümmel, F.; Löwen, H.; Bechinger, C.; Speck, T. Dynamical clustering and phase separation in suspensions of self-propelled colloidal particles. Phys. Rev. Lett. 2013, 110, 238301. (19) Kudrolli, A.; Lumay, G.; Volfson, D.; Tsimring, L. S. Swarming and swirling in self-propelled polar granular rods. Phys. Rev. Lett. 2008, 100, 058001. (20) Chen, D. T.; Lau, A.; Hough, L. A.; Islam, M. F.; Goulian, M.; Lubensky, T. C.; Yodh, A. G. Fluctuations and rheology in active bacterial suspensions. Phys. Rev. Lett. 2007, 99, 148302. (21) Narayan, V.; Ramaswamy, S.; Menon, N. Long-lived giant number fluctuations in a swarming granular nematic. Science 2007, 317, 105−108. (22) Kumar, N.; Soni, H.; Ramaswamy, S.; Sood, A. Flocking at a distance in active granular matter. Nat. Commun. 2014, 5, 4688. (23) Takatori, S. C.; De Dier, R.; Vermant, J.; Brady, J. F. Acoustic trapping of active matter. Nat. Commun. 2016, 7, 10694. (24) Nelson, B. J.; Kaliakatsos, I. K.; Abbott, J. J. Microrobots for minimally invasive medicine. Annu. Rev. Biomed. Eng. 2010, 12, 55− 85. (25) Dey, K. K.; Zhao, X.; Tansi, B. M.; Méndez-Ortiz, W. J.; Córdova-Figueroa, U. M.; Golestanian, R.; Sen, A. Micromotors powered by enzyme catalysis. Nano Lett. 2015, 15, 8311−8315. (26) Magdanz, V.; Sanchez, S.; Schmidt, O. G. Development of a sperm-flagella driven micro-bio-robot. Adv. Mater. 2013, 25, 6581− 6588. (27) Wu, Z.; Esteban-Fernández de Á vila, B.; Martín, A.; Christianson, C.; Gao, W.; Thamphiwatana, S. K.; Escarpa, A.; He, Q.; Zhang, L.; Wang, J. RBC micromotors carrying multiple cargos towards potential theranostic applications. Nanoscale 2015, 7, 13680− 13686. (28) Fischer, P.; Ghosh, A. Magnetically actuated propulsion at low Reynolds numbers: towards nanoscale control. Nanoscale 2011, 3, 557−563. (29) Ibele, M.; Mallouk, T. E.; Sen, A. Schooling Behavior of LightPowered Autonomous Micromotors in Water. Angew. Chem., Int. Ed. 2009, 48, 3308−3312. (30) Buhl, J.; Sumpter, D. J.; Couzin, I. D.; Hale, J. J.; Despland, E.; Miller, E. R.; Simpson, S. J. From disorder to order in marching locusts. Science 2006, 312, 1402−1406. (31) Rubenstein, M.; Cornejo, A.; Nagpal, R. Programmable selfassembly in a thousand-robot swarm. Science 2014, 345, 795−799. (32) Von Maltzahn, G.; Park, J.-H.; Lin, K. Y.; Singh, N.; Schwöppe, C.; Mesters, R.; Berdel, W. E.; Ruoslahti, E.; Sailor, M. J.; Bhatia, S. N. Nanoparticles that communicate in vivo to amplify tumour targeting. Nat. Mater. 2011, 10, 545. (33) Bricard, A.; Caussin, J.-B.; Das, D.; Savoie, C.; Chikkadi, V.; Shitara, K.; Chepizhko, O.; Peruani, F.; Saintillan, D.; Bartolo, D. Emergent vortices in populations of colloidal rollers. Nat. Commun. 2015, 6, 7470. I


Article

Accounts of Chemical Research (56) Walker, D.; Käsdorf, B. T.; Jeong, H.-H.; Lieleg, O.; Fischer, P. Enzymatically active biomimetic micropropellers for the penetration of mucin gels. Sci. Adv. 2015, 1, e1500501. (57) Servant, A.; Qiu, F.; Mazza, M.; Kostarelos, K.; Nelson, B. J. Controlled in vivo swimming of a swarm of bacteria-like microrobotic flagella. Adv. Mater. 2015, 27, 2981−2988. (58) Suter, M.; Zhang, L.; Siringil, E. C.; Peters, C.; Luehmann, T.; Ergeneman, O.; Peyer, K. E.; Nelson, B. J.; Hierold, C. Superparamagnetic microrobots: fabrication by two-photon polymerization and biocompatibility. Biomed. Microdevices 2013, 15, 997−1003. (59) Venugopalan, P. L.; Jain, S.; Shivashankar, S.; Ghosh, A. Single coating of zinc ferrite renders magnetic nanomotors therapeutic and stable against agglomeration. Nanoscale 2018, 10, 2327−2332. (60) Ghosh, S.; Ghosh, A. Mobile nanotweezers for active colloidal manipulation. Sci. Rob. 2018, 3, eaaq0076. (61) Hawkeye, M. M.; Brett, M. J. Glancing angle deposition: fabrication, properties, and applications of micro-and nanostructured thin films. J. Vac. Sci. Technol., A 2007, 25, 1317−1335. (62) Mandal, P.; Ghosh, A. Observation of enhanced diffusivity in magnetically powered reciprocal swimmers. Phys. Rev. Lett. 2013, 111, 248101. (63) Lauga, E.; Bartolo, D. No many-scallop theorem: Collective locomotion of reciprocal swimmers. Phys. Rev. E 2008, 78, 030901. (64) Lauga, E. Enhanced diffusion by reciprocal swimming. Phys. Rev. Lett. 2011, 106, 178101. (65) Mandal, P.; Chopra, V.; Ghosh, A. Independent positioning of magnetic nanomotors. ACS Nano 2015, 9, 4717−4725. (66) Li, T.; Zhang, A.; Shao, G.; Wei, M.; Guo, B.; Zhang, G.; Li, L.; Wang, W. Janus Microdimer Surface Walkers Propelled by Oscillating Magnetic Fields. Adv. Funct. Mater. 2018, 28, 1706066. (67) Martinez-Pedrero, F.; Tierno, P. Magnetic propulsion of selfassembled colloidal carpets: efficient cargo transport via a conveyorbelt effect. Phys. Rev. Appl. 2015, 3, 051003. (68) Li, T.; Li, J.; Zhang, H.; Chang, X.; Song, W.; Hu, Y.; Shao, G.; Sandraz, E.; Zhang, G.; Li, L.; Wang, J. Magnetically Propelled FishLike Nanoswimmers. Small 2016, 12, 6098−6105. (69) Li, T.; Li, J.; Morozov, K. I.; Wu, Z.; Xu, T.; Rozen, I.; Leshansky, A. M.; Li, L.; Wang, J. Highly efficient freestyle magnetic nanoswimmer. Nano Lett. 2017, 17, 5092−5098. (70) Wu, X.-L.; Libchaber, A. Particle diffusion in a quasi-twodimensional bacterial bath. Phys. Rev. Lett. 2000, 84, 3017.

J


Magnetic Active Matter Based on Helical Propulsion - Accounts of

Recommend Documents