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Stabilizing by steering: Enhancing bacterial motility by non-uniform diffusiophoresis

Viet Sang Doan, Ali Nikkhah, Sangwoo Shin

TL;DR

It is shown that salt gradients can be exploited to improve the run-and-tumble motility of flagellated soil bacteria, Pseudomonas putida, by biasing the cells'motion toward salt, revealing a previously unrecognized mechanism by which salt gradients can bias bacterial motility.

Abstract

Bacteria are often required to navigate across confined spaces to reach desired destinations in biological and environmental systems, allowing critical functions in host-microbe symbiosis, infection, drug delivery, soil ecology, and soil bioremediation. While the canonical run-and-tumble motility is effective in finding targets under confinement, it may not represent the most ideal strategy due to the continuous monitoring of environmental cues and stochastic recorrection of their paths. Here, we show that salt gradients can be exploited to improve the run-and-tumble motility of flagellated soil bacteria, Pseudomonas putida, by biasing the cells' motion toward salt. Salt gradients impact bacterial swimming by straightening their runs toward salt, which we attribute to diffusiophoresis acting asymmetrically around the cell. This action imposes an effective torque on the cell body that is strong enough to overcome Brownian rotation, thereby stabilizing the motion and guiding the cells toward salt with straighter runs. We further demonstrate that imposing salt gradients in the presence of toxic organic contaminants enhances their chemotactic dispersion toward the contaminants via diffusiophoresis, suggesting its potential utility in bioremediation. Our findings reveal a previously unrecognized mechanism by which salt gradients can bias bacterial motility, offering new opportunities to control microbial transport in complex environments.

Stabilizing by steering: Enhancing bacterial motility by non-uniform diffusiophoresis

TL;DR

It is shown that salt gradients can be exploited to improve the run-and-tumble motility of flagellated soil bacteria, Pseudomonas putida, by biasing the cells'motion toward salt, revealing a previously unrecognized mechanism by which salt gradients can bias bacterial motility.

Abstract

Bacteria are often required to navigate across confined spaces to reach desired destinations in biological and environmental systems, allowing critical functions in host-microbe symbiosis, infection, drug delivery, soil ecology, and soil bioremediation. While the canonical run-and-tumble motility is effective in finding targets under confinement, it may not represent the most ideal strategy due to the continuous monitoring of environmental cues and stochastic recorrection of their paths. Here, we show that salt gradients can be exploited to improve the run-and-tumble motility of flagellated soil bacteria, Pseudomonas putida, by biasing the cells' motion toward salt. Salt gradients impact bacterial swimming by straightening their runs toward salt, which we attribute to diffusiophoresis acting asymmetrically around the cell. This action imposes an effective torque on the cell body that is strong enough to overcome Brownian rotation, thereby stabilizing the motion and guiding the cells toward salt with straighter runs. We further demonstrate that imposing salt gradients in the presence of toxic organic contaminants enhances their chemotactic dispersion toward the contaminants via diffusiophoresis, suggesting its potential utility in bioremediation. Our findings reveal a previously unrecognized mechanism by which salt gradients can bias bacterial motility, offering new opportunities to control microbial transport in complex environments.

Paper Structure

This paper contains 1 equation, 5 figures.

Figures (5)

  • Figure 1: P. putida are attracted to higher salinity. (a) A microfluidic assay to evaluate cells under NaCl gradients. (b) Change in the total cell population normalized by the initial cell population over time in the presence (blue) and absence (black) of NaCl gradients. Symbols represent experimental data (blue triangles for NaCl gradients, black circles for no gradient) while solid lines represent numerical simulations. Shaded regions denote the standard deviation across three simulations. (c,d) Local distribution of cells over time (c) without (Movie S1) or (d) with NaCl gradients (Movie S2). The color code represents the number of cells in the $i$-th bin, $n_i(t)$, normalized by the total number of cells from the beginning, $\sum_i n_i(0)$.
  • Figure 2: P. putida aligns along salt gradients. (a,b) Cell trajectories recorded over 25 s of duration for different times (0--25, 75--100, 150--175 s) in the (a) absence and (b) presence of NaCl gradients. (c,d) Probability density function distribution of cell's directions of instantaneous velocity vectors in the (c) absence and (d) presence of NaCl gradients. Scale bar in (a) is 100 $\mu$m.
  • Figure 3: P. putida run faster and straighter toward salt. (a) Comparison of run speeds averaged over the entire angles, $0^\circ~(-15^\circ<\theta<15^\circ)$, and $180^\circ~(165^\circ<\theta<195^\circ)$. (b,c) Distributions of average run speed in the (b) absence and (c) presence of NaCl gradients. (d) Comparison of average run straightness for entire angles, $0^\circ~(-15^\circ<\theta<15^\circ)$, and $180^\circ~(165^\circ<\theta<195^\circ)$. (e,f) Distributions of average run straightness in the (e) absence and (f) presence of NaCl gradients. Error bars in (a,d) represent standard deviation.
  • Figure 4: Non-uniform diffusiophoresis steers P. putida toward salt. (a) An illustration of cell rotation due to non-uniform diffusiophoresis. (b,c) Experimental run trajectories (40 randomly chosen) repositioned to start at the origin in the (b) absence (Movie S3) and (c) presence (Movie S4) of NaCl gradients. The color code represents run straightness $\mathcal{S}$. (d,e) Numerical simulation run trajectories repositioned to start at the origin in the (d) absence (Movie S5) and (e) presence (Movie S6) of diffusiophoretic drift.
  • Figure 5: Salt gradients disperse cells toward toxic contaminant. (a) Simulating diffusiophoretic bioaugmentation of toluene-contaminated pore. Cells suspended in low salinity water are injected into the channel that is filled with high salinity water in the presence of toluene on the gel-sided channel, thereby creating dual chemical (salt and toluene) gradients. (b) An image of the microfluidic channel in the presence of toluene. Toluene is false-colored. (c,d) Trajectories of cells in the (c) absence (Movie S5) and (d) presence of NaCl gradients. (Movie S6) Scale bars in (b,d) are 50 $\mu$m.