Single-cell magnetotaxis in mucus-mimicking polymeric solutions

Abstract

Magnetotactic bacteria (MTB) are promising candidates for use as biomicrorobots in biomedical applications due to their motility, self-propulsion, and the ability to direct their navigation with an applied magnetic field. When in the body, the MTB may encounter non-Newtonian fluids such as blood plasma or mucus. However, their motility and the effectiveness of directed navigation in non-Newtonian fluids has yet to be studied on a single-cell level. In this work, we investigate motility of Magnetospirillum magneticum AMB-1 in three concentrations of polyacrylamide (PAM) solution, a mucus-mimicking fluid. The swimming speeds increase from 44.0 ± 13.6 μm/s in 0 mg/mL of PAM to 52.73 ± 15.6 μm/s in 1 mg/mL then decreases to 24.51 ± 11.7 μm/s in 2 mg/mL and 21.23 ± 10.5 μm/s in 3 mg/mL. This trend of a speed increase in low polymer concentrations followed by a decrease in speed as the concentration increases past a threshold concentration is consistent with other studies of motile, flagellated bacteria. Past this threshold concentration of PAM, there is a higher percentage of cells with an overall trajectory angle deviating from the angle of the magnetic field lines. There is also less linearity in the trajectories and an increase in reversals of swimming direction. Altogether, we show that MTB can be directed in polymer concentrations mimicking biological mucus, demonstrating the influence of the medium viscosity on the linearity of their trajectories which alters the effective path that could be predefined in Newtonian fluids when transport is achieved by magnetotaxis.

Keywords: magnetotactic bacteria; magnetotaxis; microfluidics; mucus; non-Newtonian fluid; polymeric solutions; viscous fluid.

Figure 1

(A) The computer-aided design of the microfluidic-electromagnetic coils platform used to produce the magnetic field for the magnetotaxis studies. (B) The simulated magnetic flux density produced by the coils for a current of 1.3 A, the current used in experiments. The white arrows indicate the direction and magnitude of the magnetic flux.

Figure 2

Shear rate vs. viscosity of PAM in concentrations of 1–6 mg/mL and gastric mucus (Curt and Pringle, 1969).

Figure 3

(A) Average bacteria swimming speed vs. PAM concentration. (B) Cell length vs. PAM concentration. The diamond markers indicate outliers. (C) The average swimming speed vs. cell length. (D) Radial plots indicating the overall trajectory angle within the ROI for each PAM concentration. The magnitude of the arrows indicates the average swimming speed during the trajectory in μm/s.

Figure 4

(A) The R² values from the linear regression of the bacteria trajectories for each PAM concentration. (B–D) The tracking overlays of individual bacteria. Arrows indicate swimming direction. Scale bar = 20 μm. (B) An example of high R², linear trajectories in 0 mg/mL PAM solution. The top trajectory in blue has an R² = 0.92 and the bottom trajectory in green has an R² = 0.94. (C) An example of a single reversal resulting in an R² value of 0.10 in 3 mg/mL PAM solution. (D) An example of a ‘wavy’ trajectory with a several short reversals that do not impact the overall direction of motion. R² = 0.34 in 2 mg/mL PAM solution.

Figure 5

(A) The percentage of bacteria with at least one reversal of direction during their trajectory for each PAM concentration. (B) The number of reversals per bacterium for each PAM concentration. Each point represents a single bacterium. (C) The tracking overlay of a bacterium in 2 mg/mL PAM solution with two reversals in its’ trajectory. (D) The tracking overlay of a bacterium in 2 mg/mL PAM solution with 14 reversals in its’ trajectory. Scale bar = 20 μm.