4.5 Article

Collective motion enhances chemotaxis in a two-dimensional bacterial swarm

Journal

BIOPHYSICAL JOURNAL
Volume 120, Issue 9, Pages 1615-1624

Publisher

CELL PRESS
DOI: 10.1016/j.bpj.2021.02.021

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Funding

  1. National Natural Science Foundation of China [11925406, 12090053, 11872358]
  2. Ministry of Science and Technology of China [2016YFA0500700]
  3. Fundamental Research Funds for the central Universities [WK2030000026]
  4. Collaborative Innovation Program of Hefei Science Center, Chinese Academy of Sciences [2019HSC-CIP004]

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When bacteria perform chemotaxis in a swarm, cell crowding enhances chemotaxis by increasing cell body alignment, leading to collective motion and increased drift velocity toward attractants. However, the enhancement of chemotaxis depends on whether the cell-cell interactions induce alignment or collisions that randomize cell moving direction in the simulation.
In a dilute liquid environment in which cell-cell interaction is negligible, flagellated bacteria, such as Escherichia coli, perform chemotaxis by biased random walks alternating between run-and-tumble. In a two-dimensional crowded environment, such as a bacterial swarm, the typical behavior of run-and-tumble is absent, and this raises the question whether and how bacteria can perform chemotaxis in a swarm. Here, by examining the chemotactic behavior as a function of the cell density, we showed that chemotaxis is surprisingly enhanced because of cell crowding in a bacterial swarm, and this enhancement is correlated with increase in the degree of cell body alignment. Cells tend to form clusters that move collectively in a swarm with increased effective run length, and we showed analytically that this resulted in increased drift velocity toward attractants. We also explained the enhancement by stochastically simulating bacterial chemotaxis in a swarm. We found that cell crowding in a swarm enhances chemotaxis if the cell-cell interactions used in the simulation induce cell-cell alignment, but it impedes chemotaxis if the interactions are collisions that randomize cell moving direction. Therefore, collective motion in a bacterial swarm enhances chemotaxis.

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