High-speed motility originates from cooperatively pushing and pulling flagella bundles in bilophotrichous bacteria

Abstract

Bacteria propel and change direction by rotating long, helical filaments, called flagella. The number of flagella, their arrangement on the cell body and their sense of rotation hypothetically determine the locomotion characteristics of a species. The movement of the most rapid microorganisms has in particular remained unexplored because of additional experimental limitations. We show that magnetotactic cocci with two flagella bundles on one pole swim faster than 500 µm·s-1 along a double helical path, making them one of the fastest natural microswimmers. We additionally reveal that the cells reorient in less than 5 ms, an order of magnitude faster than reported so far for any other bacteria. Using hydrodynamic modeling, we demonstrate that a mode where a pushing and a pulling bundle cooperate is the only possibility to enable both helical tracks and fast reorientations. The advantage of sheathed flagella bundles is the high rigidity, making high swimming speeds possible.

Data availability

3D tracks have been deposited in Dryad Digital Repository under DOI doi:10.5061/dryad.r2nd550

The following data sets were generated

Article and author information

Author details

  1. Klaas Bente

    Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Sarah Mohammadinejad

    Department of Theory and Bio-Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3758-5693
  3. Mohammad Avalin Charsooghi

    Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7772-8513
  4. Felix Bachmann

    Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Agnese Codutti

    Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher T Lefèvre

    BIAM, CEA Cadarache, Saint Paul lez Durance, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Stefan Klumpp

    Max Planck Institute of Colloids and Interfaces, Göttingen, Germany
    For correspondence
    klumpp@mpikg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
  8. Damien Faivre

    BIAM, CEA Cadarache, Saint Paul lez Durance, France
    For correspondence
    damien.faivre@cea.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6191-3389

Funding

Max-Planck-Gesellschaft (Open-access funding)

  • Damien Faivre

Deutsche Forschungsgemeinschaft (FA 835/7-2)

  • Damien Faivre

Deutsche Forschungsgemeinschaft (KL 818/2-2)

  • Stefan Klumpp

Deutscher Akademischer Austauschdienst (57314018)

  • Sarah Mohammadinejad

Deutsche Forschungsgemeinschaft (SFB 937)

  • Stefan Klumpp

Agence Nationale de la Recherche (ANR-16-TERC-0025-01)

  • Christopher T Lefèvre

IMPRS on Multiscale Biosystems (Graduate Student Fellowship)

  • Agnese Codutti

The research leading to these results was supported by the Max Planck Society and by Deutsche Forschungsgemeinschaft (DFG) within the priority program on microswimmers (grants No. KL 818/2-2 and FA 835/7-2 to S.K. and D.F.). Further, S.M. was supported by Deutscher Akademischer Austauschdienst, DAAD (grant no. 57314018) as well as Deutsche Forschungsgemeinschaft (DFG) through SFB 937. A.C. is funded by the IMPRS on Multiscale Biosystems. C.T.L acknowledges support by the French National Research Agency (ANR Tremplin-ERC: ANR-16-TERC-0025-01).

Reviewing Editor

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

Version history

  1. Received: April 9, 2019
  2. Accepted: January 27, 2020
  3. Accepted Manuscript published: January 28, 2020 (version 1)
  4. Version of Record published: February 10, 2020 (version 2)

Copyright

© 2020, Bente 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. Klaas Bente
  2. Sarah Mohammadinejad
  3. Mohammad Avalin Charsooghi
  4. Felix Bachmann
  5. Agnese Codutti
  6. Christopher T Lefèvre
  7. Stefan Klumpp
  8. Damien Faivre
(2020)
High-speed motility originates from cooperatively pushing and pulling flagella bundles in bilophotrichous bacteria
eLife 9:e47551.
https://doi.org/10.7554/eLife.47551

Share this article

https://doi.org/10.7554/eLife.47551

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