Interplay of surface interaction and magnetic torque in single-cell motion of magnetotactic bacteria in microfluidic confinement

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    Evaluation Summary:

    The manuscript reports results of a combined experimental and numerical investigation of magnetotactic bacteria in strong spatial confinement and under the influence of an external magnetic field. Single cells are trapped in micrometer-sized microfluidic chambers. A variety of trajectories are found, which depend on the chamber size and the strength of the magnetic field. A detailed understanding of swimming in simple controlled confinement is essential to predict the behavior of motile microorganisms in the complex environments of their natural habitat.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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Abstract

Swimming microorganisms often experience complex environments in their natural habitat. The same is true for microswimmers in envisioned biomedical applications. The simple aqueous conditions typically studied in the lab differ strongly from those found in these environments and often exclude the effects of small volume confinement or the influence that external fields have on their motion. In this work, we investigate magnetically steerable microswimmers, specifically magnetotactic bacteria, in strong spatial confinement and under the influence of an external magnetic field. We trap single cells in micrometer-sized microfluidic chambers and track and analyze their motion, which shows a variety of different trajectories, depending on the chamber size and the strength of the magnetic field. Combining these experimental observations with simulations using a variant of an active Brownian particle model, we explain the variety of trajectories by the interplay between the wall interactions and the magnetic torque. We also analyze the pronounced cell-to-cell heterogeneity, which makes single-cell tracking essential for an understanding of the motility patterns. In this way, our work establishes a basis for the analysis and prediction of microswimmer motility in more complex environments.

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  1. Evaluation Summary:

    The manuscript reports results of a combined experimental and numerical investigation of magnetotactic bacteria in strong spatial confinement and under the influence of an external magnetic field. Single cells are trapped in micrometer-sized microfluidic chambers. A variety of trajectories are found, which depend on the chamber size and the strength of the magnetic field. A detailed understanding of swimming in simple controlled confinement is essential to predict the behavior of motile microorganisms in the complex environments of their natural habitat.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

  2. Reviewer #1 (Public Review):

    The authors present results of experiments and computer simulations of magnetotactic bacteria confined within sealed microfluidic devices. They isolate a single cell within circular compartments and track its motion over long periods of time, to study its statistical properties. Following previous work on microalgae, the present authors study the behavior of the radial distribution function of the bacterial cells for difference confining radii, and also in the absence/presence of a magnetic field. The inclusion of a magnetic field produces qualitatively different trajectories on account of the reorienting magnetic torque leading e..g to U-turn-like motion.

    This work adds interesting results to the characterization of microbial motility at the single cell level for a class of cells with important potential applications: magnetotactic bacteria.

    The conclusions of this manuscript are well supported by the evidence provided. Some weaknesses of the analysis is that there is no clear discussion of the interactions among cells when more than one are trapped within the same fluidic chamber. The authors could have separated contribution from isolated cells from the pairs or triplets of cells in the radial distribution function to measure the role of cell-cell interactions.

    The methods used in both experimental and simulation analysis are adequate and useful to the community. Comparing, as they do, the results of this manuscript with the work on microalgae by Ostapenko et al., the present authors demonstrate that features of single-cell motion in confinement do not depend sensitively on the details of the propulsion mechanism. This aspect of this work will have considerable impact in the field, beyond the importance to magnetotactic cells.

  3. Reviewer #2 (Public Review):

    The manuscript reports results of a combined experimental and numerical investigation of magnetotactic bacteria in strong spatial confinement and under the influence of an external magnetic field. Single cells are trapped in micrometer-sized microfluidic chambers and their motion is analyzed. A variety of different trajectories are found, which depend on the chamber size and the strength of the magnetic field. Simulations of a model of active Brownian spheres helps to explain the variety of trajectories by the interplay between the wall interactions and the magnetic torque. A pronounced cell-to-cell heterogeneity is observed.

    The swimming behavior without magnetic field is found to be very similar to the previously observed swimming of algae in a circular environment, i.e. with the microswimmers moving along the wall, see Ref.[31]. In the current study, a magnetic field can be used as an additional external control parameter, which leads to U-turns inside the trap to reorient bacteria in the field direction.