A Tad-like apparatus is required for contact-dependent prey killing in predatory social bacteria

  1. Sofiene Seef
  2. Julien Herrou
  3. Paul de Boissier
  4. Laetitia My
  5. Gael Brasseur
  6. Donovan Robert
  7. Rikesh Jain
  8. Romain Mercier
  9. Eric Cascales
  10. Bianca H Habermann
  11. Tâm Mignot  Is a corresponding author
  1. CNRS-Aix Marseille University, France
  2. Aix-Marseille Université - CNRS UMR 7288,, France
  3. Centre national de la recherche scientifique - Aix-Marseille Université, France

Abstract

Myxococcus xanthus, a soil bacterium, predates collectively using motility to invade prey colonies. Prey lysis is mostly thought to rely on secreted factors, cocktails of antibiotics and enzymes, and direct contac with Myxococcus cells. In this study, we show that on surfaces the coupling of A-motility and contact-dependent killing is the central predatory mechanism driving effective prey colony invasion and consumption. At the molecular level, contact-dependent killing involves a newly discovered type IV filament-like machinery (Kil) that both promotes motility arrest and prey cell plasmolysis. In this process, Kil proteins assemble at the predator-prey contact site, suggesting that they allow tight contact with prey cells for their intoxication. Kil-like systems form a new class of Tad-like machineries in predatory bacteria, suggesting a conserved function in predator-prey interactions. This study further reveals a novel cell-cell interaction function for bacterial pili-like assemblages.

Data availability

Source Data files have been provided for :- Figure 2-source data 1: E. coli loss of fluorescence during contact-dependent lysis (Figure 2c).- Figure 2-figure supplement 5-source data 1: Contact dependent-lysis and VipA-GFP dynamics.- Figure 2-figure supplement 7-source data 1: CPRG assay.- Figure 3-source data 1: CPRG assay (Figure 3b).- Figure 3-source data 2: counting percentage of contacts with a prey leading to motility pauses and prey cell lysis (Figure 3c, 3d).- Figure 3-figure supplement 3-source data 1: CPRG assay.- Figure 4-source data 1: counting percentage of contacts with a prey leading to NG-KilD foci formation and counting percentage of NG-KilD foci associated with motility pause and prey cell lysis (Figure 4e, 4f, 4g).- Figure 4-figure supplement 1-source data 1: CPRG assay.- Figure 4-figure supplement 2-source data 1: CPRG assay.- Figure 4-figure supplement 3-source data 1: Lysis time.- Figure 4-figure supplement 4-source data 1: Western Blot.- Figure 5-source data 1: Flow cytometry (Figure 5c, 5d).- Figure 5-source data 2: M. xanthus growth during prey colony invasion (Figure 5e).- Figure 5-source data 3: Increase in M. xanthus cell length during predation (Figure 5f).- Figure 5-figure supplement 2-source data 1: Growth curves.- Figure 6-source data 1: Prey CFU counts during predation (Figure 6b,c,d,e,f).- Figure 7-source data 1: Supermatrix alignment.- Figure 3-figure supplement 2: RNA-seq Data from Livingstone PG et al. (2018) Microb Genom. PMID:29345219, Supplementary File 1 available online: https://www.microbiologyresearch.org/content/journal/mgen/10.1099/mgen.0.000152#supplementary_data).

The following previously published data sets were used

Article and author information

Author details

  1. Sofiene Seef

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  2. Julien Herrou

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  3. Paul de Boissier

    Institut de Biologie du Développement de Marseille and Turing Center for Living Systems, Aix-Marseille Université - CNRS UMR 7288,, Marseille, France
    Competing interests
    No competing interests declared.
  4. Laetitia My

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7876-1809
  5. Gael Brasseur

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  6. Donovan Robert

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  7. Rikesh Jain

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  8. Romain Mercier

    CNRS-Aix Marseille University, Marseille, France
    Competing interests
    No competing interests declared.
  9. Eric Cascales

    Mediterranean Institute of Microbiology, Centre national de la recherche scientifique - Aix-Marseille Université, Marseille, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0611-9179
  10. Bianca H Habermann

    Computational Biology Group, Aix-Marseille Université - CNRS UMR 7288,, Marseille, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2457-7504
  11. Tâm Mignot

    CNRS-Aix Marseille University, Marseille, France
    For correspondence
    tmignot@imm.cnrs.fr
    Competing interests
    Tâm Mignot, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4338-9063

Funding

Centre National de la Recherche Scientifique (2019 CNRS 80-Prime)

  • Tâm Mignot

Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)

  • Sofiene Seef

Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)

  • Paul de Boissier

Ministère de l'Éducation et de l'Enseignement supérieur (MENRT thesis grant)

  • Donovan Robert

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

Reviewing Editor

  1. Michael T Laub, Massachusetts Institute of Technology, United States

Publication history

  1. Preprint posted: February 27, 2021 (view preprint)
  2. Received: July 22, 2021
  3. Accepted: September 9, 2021
  4. Accepted Manuscript published: September 10, 2021 (version 1)
  5. Version of Record published: September 23, 2021 (version 2)

Copyright

© 2021, Seef 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. Sofiene Seef
  2. Julien Herrou
  3. Paul de Boissier
  4. Laetitia My
  5. Gael Brasseur
  6. Donovan Robert
  7. Rikesh Jain
  8. Romain Mercier
  9. Eric Cascales
  10. Bianca H Habermann
  11. Tâm Mignot
(2021)
A Tad-like apparatus is required for contact-dependent prey killing in predatory social bacteria
eLife 10:e72409.
https://doi.org/10.7554/eLife.72409

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