Confinement discerns swarmers from planktonic bacteria

  1. Weijie Chen
  2. Neha Mani
  3. Hamid Karani
  4. Hao Li
  5. Sridhar Mani
  6. Jay X Tang  Is a corresponding author
  1. Brown University, United States
  2. Albert Einstein College of Medicine, United States

Abstract

Powered by flagella, many bacterial species exhibit collective motion on a solid surface commonly known as swarming. As a natural example of active matter, swarming is also an essential biological phenotype associated with virulence, chemotaxis, and host pathogenesis. Physical changes like cell elongation and hyper flagellation have been shown to accompany the swarming phenotype. Less studied, however, are the contrasts of collective motion between the swarming cells and their counterpart planktonic cells of comparable cell density. Here, we show that confining bacterial movement in circular microwells allows distinguishing bacterial swarming from collective swimming. On a soft agar plate, a novel bacterial strain Enterobacter sp. SM3 in swarming and planktonic states exhibited different motion patterns when confined to circular microwells of a specific range of sizes. When the confinement diameter was between 40 μm and 90 μm, swarming SM3 formed a single swirl motion pattern in the microwells whereas planktonic SM3 formed multiple swirls. Similar differential behavior is observed across several other species of gram-negative bacteria. We also observed 'rafting behavior' of swarming bacteria upon dilution. We hypothesize that the rafting behavior might account for the motion pattern difference. We were able to predict these experimental features via numerical simulations where swarming cells are modeled with stronger cell-cell alignment interaction. Our experimental design using PDMS microchip disk arrays enabled us to observe bacterial swarming on murine intestinal surface suggesting a new method for characterizing bacterial swarming under complex environments, such as in polymicrobial niches, and for in vivo swarming exploration.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source code files have been provided for Figure 5.

Article and author information

Author details

  1. Weijie Chen

    Brown University, Providence, United States
    Competing interests
    Weijie Chen, Weijie Chen, Neha Mani, Jay X. Tang, and Sridhar Mani filed a U.S. patent application (Application No. 63033369)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7105-5645
  2. Neha Mani

    Brown University, Providence, United States
    Competing interests
    Neha Mani, Weijie Chen, Neha Mani, Jay X. Tang, and Sridhar Mani filed a U.S. patent application (Application No. 63033369)..
  3. Hamid Karani

    Brown University, Providence, United States
    Competing interests
    No competing interests declared.
  4. Hao Li

    Albert Einstein College of Medicine, New York, United States
    Competing interests
    No competing interests declared.
  5. Sridhar Mani

    Albert Einstein College of Medicine, New York, United States
    Competing interests
    Sridhar Mani, Weijie Chen, Neha Mani, Jay X. Tang, and Sridhar Mani filed a U.S. patent application (Application No. 63033369)..
  6. Jay X Tang

    Brown University, Providence, United States
    For correspondence
    jay_tang@brown.edu
    Competing interests
    Jay X Tang, Weijie Chen, Neha Mani, Jay X. Tang, and Sridhar Mani filed a U.S. patent application (Application No. 63033369)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1022-4337

Funding

National Institutes of Health (R01CA222469)

  • Sridhar Mani

National Institutes of Health (ES030197)

  • Sridhar Mani

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Ethics

Animal experimentation: The animal tissue samples were acquired from Albert Einstein College of Medicine in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. This study was approved by the Institute of Animal Studies at the Albert Einstein College of Medicine, Inc (IACUC # 20160706 & 00001172).

Version history

  1. Received: October 22, 2020
  2. Accepted: April 21, 2021
  3. Accepted Manuscript published: April 22, 2021 (version 1)
  4. Version of Record published: May 11, 2021 (version 2)

Copyright

© 2021, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Weijie Chen
  2. Neha Mani
  3. Hamid Karani
  4. Hao Li
  5. Sridhar Mani
  6. Jay X Tang
(2021)
Confinement discerns swarmers from planktonic bacteria
eLife 10:e64176.
https://doi.org/10.7554/eLife.64176

Share this article

https://doi.org/10.7554/eLife.64176

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