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The mechanism of force transmission at bacterial focal adhesion complexes

Author

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  • Laura M. Faure

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Jean-Bernard Fiche

    (Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Montpellier University)

  • Leon Espinosa

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Adrien Ducret

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée
    Indiana University)

  • Vivek Anantharaman

    (National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • Jennifer Luciano

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Sébastien Lhospice

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Salim T. Islam

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Julie Tréguier

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Mélanie Sotes

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

  • Erkin Kuru

    (Interdisciplinary Biochemistry Program, Indiana University)

  • Michael S. Van Nieuwenhze

    (Indiana University)

  • Yves V. Brun

    (Indiana University)

  • Olivier Théodoly

    (Adhesion and Inflammation laboratory, INSERM U1067, Aix Marseille University)

  • L. Aravind

    (National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • Marcelo Nollmann

    (Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Montpellier University)

  • Tâm Mignot

    (Laboratoire de Chimie Bactérienne, CNRS-Aix Marseille University UMR7283, Institut de Microbiologie de la Méditerranée)

Abstract

Various rod-shaped bacteria mysteriously glide on surfaces in the absence of appendages such as flagella or pili. In the deltaproteobacterium Myxococcus xanthus, a putative gliding motility machinery (the Agl–Glt complex) localizes to so-called focal adhesion sites (FASs) that form stationary contact points with the underlying surface. Here we show that the Agl–Glt machinery contains an inner-membrane motor complex that moves intracellularly along a right-handed helical path; when the machinery becomes stationary at FASs, the motor complex powers a left-handed rotation of the cell around its long axis. At FASs, force transmission requires cyclic interactions between the molecular motor and the adhesion proteins of the outer membrane via a periplasmic interaction platform, which presumably involves contractile activity of motor components and possible interactions with peptidoglycan. Our results provide a molecular model of bacterial gliding motility.

Suggested Citation

  • Laura M. Faure & Jean-Bernard Fiche & Leon Espinosa & Adrien Ducret & Vivek Anantharaman & Jennifer Luciano & Sébastien Lhospice & Salim T. Islam & Julie Tréguier & Mélanie Sotes & Erkin Kuru & Michae, 2016. "The mechanism of force transmission at bacterial focal adhesion complexes," Nature, Nature, vol. 539(7630), pages 530-535, November.
  • Handle: RePEc:nat:nature:v:539:y:2016:i:7630:d:10.1038_nature20121
    DOI: 10.1038/nature20121
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    Cited by:

    1. Sara Rombouts & Anna Mas & Antoine Gall & Jean-Bernard Fiche & Tâm Mignot & Marcelo Nollmann, 2023. "Multi-scale dynamic imaging reveals that cooperative motility behaviors promote efficient predation in bacteria," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Luís António Menezes Carreira & Filipe Tostevin & Ulrich Gerland & Lotte Søgaard-Andersen, 2020. "Protein-protein interaction network controlling establishment and maintenance of switchable cell polarity," PLOS Genetics, Public Library of Science, vol. 16(6), pages 1-30, June.
    3. Salim T Islam & Israel Vergara Alvarez & Fares Saïdi & Annick Guiseppi & Evgeny Vinogradov & Gaurav Sharma & Leon Espinosa & Castrese Morrone & Gael Brasseur & Jean-François Guillemot & Anaïs Benarouc, 2020. "Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion," PLOS Biology, Public Library of Science, vol. 18(6), pages 1-31, June.

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