Propulsion and Chemotaxis in Bacteria-Driven Microswimmers.

Jiang Zhuang,Metin Sitti,Byung-Wook Park

doi:10.1002/advs.201700109

Abstract

Despite the large body of experimental work recently on biohybrid microsystems, few studies have focused on theoretical modeling of such systems, which is essential to understand their underlying functioning mechanisms and hence design them optimally for a given application task. Therefore, this study focuses on developing a mathematical model to describe the 3D motion and chemotaxis of a type of widely studied biohybrid microswimmer, where spherical microbeads are driven by multiple attached bacteria. The model is developed based on the biophysical observations of the experimental system and is validated by comparing the model simulation with experimental 3D swimming trajectories and other motility characteristics, including mean squared displacement, speed, diffusivity, and turn angle. The chemotaxis modeling results of the microswimmers also agree well with the experiments, where a collective chemotactic behavior among multiple bacteria is observed. The simulation result implies that such collective chemotaxis behavior is due to a synchronized signaling pathway across the bacteria attached to the same microswimmer. Furthermore, the dependencies of the motility and chemotaxis of the microswimmers on certain system parameters, such as the chemoattractant concentration gradient, swimmer body size, and number of attached bacteria, toward an optimized design of such biohybrid system are studied. The optimized microswimmers would be used in targeted cargo, e.g., drug, imaging agent, gene, and RNA, transport and delivery inside the stagnant or low‐velocity fluids of the human body as one of their potential biomedical applications.

Highlights

Despite the large body of experimental work recently on biohybrid microellated swimming bacteria can efficiently systems, few studies have focused on theoretical modeling of such systems, convert chemical energy into mechanical which is essential to understand their underlying functioning mechanisms and design them optimally for a given application task
Flagella morphology is another important consideration in the bacterial propulsion model, because it determines the propelling forces exerted on the microswimmer
Following from this assumption, the attached bacteria can be modeled as a finite state machine with two states, running and tumbling, and the transition between these two states are determined by their chemical signaling pathway, discussed in the subsection

Summary

Multicellular Propulsion Model

Most of the studies on bacteria-driven microswimmers adopt a similar design, which is a sphere-shaped microbead driven by single or multiple flagellated bacteria attached to it in random locations and orientations.[2,6,9,11,12,13,14,17,20,21,22,23,24,25] This particular design is chosen for its easier fabrication, characterization, and analysis, and isotropic physical properties, such as drag coefficient, in all orientations. Scanning electron microscope (SEM) images (Figure 1a) show that bacteria typically attach to spherical surfaces on their sides or with a small tilt angle, but other than that, the attachment orientation of bacteria is purely random Flagella morphology is another important consideration in the bacterial propulsion model, because it determines the propelling forces exerted on the microswimmer. The bacterial flagella could have more complicated morphologies over bacterial propulsion, based on the available observations, we conjecture that a “bundle-and-unbundle” dynamics, corresponding to the bacterial “run-and-tumble” motility, could still be the dominant flagellar morphology transition pattern Following from this assumption, the attached bacteria can be modeled as a finite state machine with two states, running and tumbling, and the transition between these two states are determined by their chemical signaling pathway, discussed in the subsection. Considering the spherical rigid body in our model, instantaneous fluid drag force (Fdrag) and torque (Tdrag) can be expressed in terms of the velocity and the angular velocity of the moving sphere, respectively, as follows. At each time step of the model simulation, rigid body translation and rotation are performed for the sphere and the attached bacteria to update their positions and orientations

Bacterial Chemotaxis Model

Chemotaxis of Multicellular Microswimmers

Discussion

Experimental Section

Conflict of Interest