Acoustic microbubble propulsion, train-like assembly and cargo transport

Article https://doi.org/10.1038/s41467-023-40387-7 Acoustic microbubble propulsion, train-like assembly and cargo transport Received: 31 December 2021 Accepted: 20 July 2023 1234567890():,; 1234567890():,; Check for updates Jakub Janiak1, Yuyang Li Daniel Ahmed 1 1,2 , Yann Ferry1,2, Alexander A. Doinikov 1 & Achieving controlled mobility of microparticles in viscous fluids can become pivotal in biologics, biotechniques, and biomedical applications. The selfassembly, trapping, and transport of microparticles are being explored in active matter, micro and nanorobotics, and microfluidics; however, little work has been done in acoustics, particularly in active matter and robotics. This study reports the discovery and characterization of microbubble behaviors in a viscous gel that is confined to a slight opening between glass boundaries in an acoustic field. Where incident waves encounter a narrow slit, acoustic pressure is amplified, causing the microbubbles to nucleate and cavitate within it. Intermittent activation transforms microbubbles from spherical to ellipsoidal, allowing them to be trapped within the interstice. Continuous activation propels ellipsoidal microbubbles through shape and volume modes that is developed at their surfaces. Ensembles of microbubbles self-assemble into a train-like arrangement, which in turn capture, transport, and release microparticles. Achieving controlled mobility of microparticles and microbubbles in viscous fluids and gel-like media can create exciting new opportunities in the natural and life sciences and open up novel biotechniques and biomedical applications. However, while manipulation of microparticles in viscous gel is both important and challenging1–11, little work has been done on this subject. Typically, microparticle mobility has been achieved, generally by (1) applying external-field gradients and (2) instituting nonreciprocal motion, such as a spiraling motion, within a designed microstructure. The first demonstrated manipulation of dielectric microparticles, using optical tweezers, operated on a tightlyfocused gradient of light7,8. Later, magnetic9, acoustic10–20, and electric21 field gradients were adopted. Acoustic-22–32, electric-33,34, magnetic-35–44, and light-45 based approaches can also initiate propulsion by exploiting nonreciprocity within a microstructure or any appendages anchored to it. However, to date, most manipulation and propulsion of microparticles and microarchitectures has been executed in a simple viscous fluid, i.e., water. Although nature’s microswimmers such as bacteria46, spirochetes47, and spermatozoa48 can navigate effectively in complex fluids and gel-like media, their artificial counterparts find viscous fluids extremely challenging. Only a few synthetic microswimmers have achieved navigation in viscous fluids49,50, such as a magnetic “micro-scallop” that is propelled through the back and forth, i.e., reciprocal, motion of its appendages51. Other magnetic designs have been studied for navigating through bodily fluids52,53 and the vitreous humor of the eye54. In addition, an acoustic vortex beam was recently developed to trap and manipulate microbubbles inside agarose gels55. Another important feature of microrobots is their ability to trap and transport microparticles; however, till date, most artificial swimmers demonstrate trapping in a water-like medium. Herein we report the discovery of various microbubble behaviors in an acoustic field when confined to shallow openings between two glass boundaries in a shear-thinning gel. We observed microbubble nucleation due to intensification of incident acoustic waves at the narrow slit; theoretical development of the pressure field across the glass boundaries supported this acoustic amplification. When the acoustic field was turned off, the microbubbles moved to the sides. Peculiarly, when dormant microbubbles located outside the opening 1 Acoustic Robotics Systems Lab (ARSL), Institute of Robotics and Intelligent Systems, ETH Zurich, CH-8803 Rüschlikon, Switzerland. 2These authors cone-mail: tributed equally: Yuyang Li, Yann Ferry. Nature Communications | (2023)14:4705 1 Article https://doi.org/10.1038/s41467-023-40387-7 were exposed to ultrasound, they squeezed through the shallow slit, transforming shape from spherical to discoidal just milliseconds prior, and consequently became trapped. Both single and multiple microbubbles were observed to execute controlled propulsion upon activation, the driving mechanism of which we believe stems from superposition of volume and high-amplitude surface modes developed at the microbubble skin. As individual microbubbles approached each other, they self-assembled into a train and traveled in unison at uniform velocity. Surprisingly, when we injected solid microparticles into the surrounding environment, they became trapped between members of the bubble microtrain. Finally, after the train arrived at a destination, the transducer was deactivated and the trapped microparticles released. Our system thus mimics a cargo train at microscale. We envision that acoustically-activated microbubbles can be a implemented in the position manipulation of microparticles in viscous fluids. The developed platform has a number of prospective uses, such as the controlled manipulation, enrichment, and separation of microparticles in extremely viscous fluids for microfluidic applications and also for applications in biologics and life sciences, for example the investigation of chemotaxis at single-cell resolution in a gel-like medium; extraction and enrichment of cells and exosomes from viscous bodily fluids for lung cancer biomarkers1,3,6,56–58; targeted inoculation of cells in gel-mimetic extracellular matrices59,60, among others. Results Experimental setup Our experimental design incorporates a piezo disc transducer mounted on a glass slide, as shown in the schematic in Fig. 1a. An electronic function generator drives the transducer to produce vibration in the glass slide. We activated the transducer’s thickness mode at excitation frequencies of 22.3−23 kHz and amplitude 20–40 VPP. A viscous, shearthinning gel was applied to the glass slide ~5–15 mm away from the transducer. A glass capillary with a circular cross-section was then placed on top of the gel and pressed down until bubbles began to nucleate and cavitate in the interstice; see Figs. 1b, c and S1. The entire setup was placed on an inverted microscope connected to a highly sensitive, high-speed camera to study the behaviors of microbubbles within the confines of the narrow aperture (see also Fig. 1d and “Materials and methods”). Modeling of acoustic pressure across a narrow slit A theoretical model across the narrow slit has been developed that explains the physical mechanism behind the experimental effects we observed. The model approximates the physical situation under study as follows. It is assumed that there are two closely-spaced cylinders, of which the bigger cyli (...truncated)