Escape problem of magnetotactic bacteria - physiological magnetic field strengths help magnetotactic bacteria navigate in simulated sediments

  1. Agnese Codutti
  2. Mohammad A. Charsooghi
  3. Konrad Marx
  4. Elisa Cerdá-Doñate
  5. Omar Munoz
  6. Paul Zaslansky
  7. Vitali Telezki
  8. Tom Robinson
  9. Damien Faivre
  10. Stefan Klumpp

  • Curated by eLife

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    eLife assessment

    This study presents valuable experimental and numerical results on the motility of a magnetotactic bacterium living in sedimentary environments, particularly in environments of varying magnetic field strengths. The evidence supporting the claims of the authors is solid, although the statistical significance comparing experiments with the numerical work is weak. The study will be of interest to biophysicists interested in bacterial motility.

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Abstract

Bacterial motility is typically studied in bulk solution, while their natural habitats often are complex environments. Here, we produced microfluidic channels that contained sediment-mimicking obstacles to study swimming of magnetotactic bacteria in a near-realistic environment. Magnetotactic bacteria are microor-ganisms that form chains of nanomagnets and that orient in Earth’s magnetic field. The obstacles were produced based on micro-computer tomography reconstructions of bacteria-rich sediment samples. We characterized the swimming of the cells through these channels and found that swimming throughput was highest for physiological magnetic fields. This observation was confirmed by extensive computer simulations using an active Brownian particle model, which were parameterized based on experimental trajectories, in particular with the trajectories near the sediment-mimicking obstacles, from which the interactions of the swimming bacteria with the obstacles were determined. The simulations were used to quantify the swimming throughput in detail. They showed the behavior seen in experiments, but also exhibited considerable variability between different channel geometries. The simulations indicate that swimming at strong fields is impeded by the trapping of bacteria in “corners” that require transient swimming against the magnetic field for escape. At weak fields, the direction of swimming is almost random, making the process inefficient as well. We confirmed the trapping effect in our experiments and showed that lowering the field strength allows the bacteria to escape. We hypothesize that over the course of evolution, magnetotactic bacteria have thus evolved to produce magnetic properties that are adapted to the geomagnetic field in order to balance movement and orientation in such crowded environments.

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  1. Version published to 10.1101/2023.12.08.570788v2 on bioRxiv
  2. eLife

    eLife assessment

    This study presents valuable experimental and numerical results on the motility of a magnetotactic bacterium living in sedimentary environments, particularly in environments of varying magnetic field strengths. The evidence supporting the claims of the authors is solid, although the statistical significance comparing experiments with the numerical work is weak. The study will be of interest to biophysicists interested in bacterial motility.

  3. eLife

    Reviewer #1 (Public Review):

    Summary:
    The authors present experimental and numerical results on the motility Magnetospirillum gryphiswaldense MSR-1, a magnetotactic bacterium living in sedimentary environments. The authors manufactured microfluidic chips containing three-dimensional obstacles of irregular shape, that match the statistical features of the grains observed in the sediment via micro-computer tomography. The bacteria are furthermore subject to an external magnetic field, whose intensity can be varied. The key quantity measured in the experiments is the throughput ratio, defined as the ratio between the number of bacteria that reach the end of the microfluidic channel and the number of bacteria entering it. The main result is that the throughput ratio is non-monotonic and exhibits a maximum at magnetic field strength comparable with Earth's magnetic field. The authors rationalize the throughput suppression at large magnetic fields by quantifying the number of bacteria trapped in corners between grains.

    Strengths:
    While magnetotactic bacteria's general motility in bulk has been characterized, we know much less about their dynamics in a realistic setting, such as a disordered porous material. The micro-computer tomography of sediments and their artificial reconstruction in a microfluidic channel is a powerful method that establishes the rigorous methodology of this work. This technique can give access to further characterization of microbial motility. The coupling of experiments and computer simulations lends considerable strength to the claims of the authors, because the model parameters (with one exception) are directly measured in the experiments.

    Weaknesses:
    The main weakness of the manuscript pertains to the discussion of the statistical significance of the experimental throughput ratio. Especially when comparing results at zero and 50 micro Tesla. The simulations seem to predict a stronger effect than seen in the experiments. The authors do not address this discrepancy.

  4. eLife

    Reviewer #2 (Public Review):

    Summary:
    simulation study of magnetotactic bacteria in microfluidic channels containing sediment-mimicking obstacles. The obstacles were produced based on micro-computer tomography reconstructions of bacteria-rich sediment samples. The swimming of bacteria through these channels is found experimentally to display the highest throughput for physiological magnetic fields. Computer simulations of active Brownian particles, parameterized based on experimental trajectories are used to quantify the swimming throughput in detail. Similar behavior as in experiments is obtained, but also considerable variability between different channel geometries. Swimming at strong field is impeded by the trapping of bacteria in corners, while at weak fields the direction of motion is almost random. The trapping effect is confirmed in the experiments, as well as the escape of bacteria with reducing field strength.

    Strengths:
    This is a very careful and detailed study, which draws its main strength from the fruitful combination of the construction of novel microfluidic devices, their use in motility experiments, and simulations of active Brownian particles adapted to the experiment. Based on their results, the authors hypothesize that magnetotactic bacteria may have evolved to produce magnetic properties that are adapted to the geomagnetic field in order to balance movement and orientation in such crowded environments. They provide strong arguments in favor
    of such a hypothesis.

    Weaknesses:
    Some of the issues touched upon here have been studied also in other articles. It would be good to extend the list of references accordingly and discuss the relation briefly in the text.

  5. Version published to 10.7554/elife.98001 on eLife
  6. Version published to 10.7554/elife.98001.1 on eLife
  7. Version published to 10.1101/2023.12.08.570788v1 on bioRxiv