Chemotaxis of bio-hybrid multiple bacteria-driven microswimmers

Abstract

In this study, in a bio-hybrid microswimmer system driven by multiple Serratia marcescens bacteria, we quantify the chemotactic drift of a large number of microswimmers towards L-serine and elucidate the associated collective chemotaxis behavior by statistical analysis of over a thousand swimming trajectories of the microswimmers. The results show that the microswimmers have a strong heading preference for moving up the L-serine gradient, while their speed does not change considerably when moving up and down the gradient; therefore, the heading bias constitutes the major factor that produces the chemotactic drift. The heading direction of a microswimmer is found to be significantly more persistent when it moves up the L-serine gradient than when it travels down the gradient; this effect causes the apparent heading preference of the microswimmers and is the crucial reason that enables the seemingly cooperative chemotaxis of multiple bacteria on a microswimmer. In addition, we find that their chemotactic drift velocity increases superquadratically with their mean swimming speed, suggesting that chemotaxis of bio-hybrid microsystems can be enhanced by designing and building faster microswimmers. Such bio-hybrid microswimmers with chemotactic steering capability may find future applications in targeted drug delivery, bioengineering, and lab-on-a-chip devices.

Propulsion and Chemotaxis in Bacteria‐Driven Microswimmers

“…The simulated drifting process, however, appears to be faster than the experimental one, reaching a steady state distribution after 4 min as compared to 8 min for experiment; this could be resulted from the fact that, compared with a simulated ideal system, the experimental system of microswimmers bears various imperfections, such as the existence of non‐motile instances and the aggregations of microswimmers. The analysis on the simulated trajectories suggests that the swimming direction of a microswimmer is more persistent when it travels up the gradient than when it moves reversely, and this is consistent with experimental observations 24, 25. When projected onto one axis, such biased motion can be quantified by the “relative reversing rate bias,”24 defining the bias in the direction reversing rate over the heading of an object performing an 1D random walk; the quantity contributes to the chemotactic drift velocity as a linear factor 51.…”

“…The simulations of the model produces 3D trajectories and motility characteristics that resemble those of experiments. The model, in combination with the signaling pathway models of bacterial chemotaxis, also traces out the chemotaxis behavior of bacteria‐driven microswimmers reported by recent studies 14, 17, 20, 21, 22, 23, 24, 25. The agreement between simulation and experiment implies that our model assumptions are reasonable and the model captures the fundamental biophysical mechanisms of the system.…”

“…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 also isotropic physical properties, such as drag coefficient, in all orientations.…”

“…Over the past decade, numerous studies have been conducted on harnessing the flagellated bacteria, such as E. coli and S. marcescens , as propellers for biohybrid microswimmers,1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17 aiming to develop a new type of targeted drug delivery system for tumor therapy 14, 16, 18, 19. Recently, efforts have also been made to guide the motion of such bacteria‐driven microswimmers through taxis‐based14, 17, 20, 21, 22, 23, 24, 25 and magnetic steering16, 26 approaches. Among these studies, the most common way to integrate bacteria into biohybrid microswimmers is attaching intact bacterial cells onto the surfaces of synthetic microstructures, such as polystyrene microbeads, where the attachment could be enabled either by physical attraction2 or through chemical bonding 14.…”

“…Such natural sensing abilities of bacteria are considered to be ideal guiding mechanisms for the motion of biohybrid microsystems, especially for healthcare applications in the human body, where chemical cues are ubiquitous. Thus far, the taxis‐based guiding method constitutes the major way to regulate the otherwise highly stochastic motion of bacteria‐driven microswimmers, which has been studied both in vitro17, 20, 21, 22, 23, 24, 25 and in vivo 14, 16. Chemotaxis, one of the most common taxis behaviors in bacteria, has been well understood36 and its signaling pathway has been mathematically modeled 37, 38, 39, 40, 41, 42, 43.…”