A mobile genetic element increases bacterial host fitness by manipulating development

  1. Joshua M Jones
  2. Ilana Grinberg
  3. Avigdor Eldar  Is a corresponding author
  4. Alan D Grossman  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
  2. Tel Aviv University, Israel

Abstract

Horizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICEBs1, an integrative and conjugative element of Bacillus subtilis, provides to its host cells. Activation of ICEBs1 conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICEBs1-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICEBs1 gene, devI (formerly ydcO), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICEBs1 to increase host fitness, thereby increasing propagation of the element.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures

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Author details

  1. Joshua M Jones

    Department of Biology, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3327-8899
  2. Ilana Grinberg

    The Shmunis School of Biomedicine and Cancer Research, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Avigdor Eldar

    School of Molecular Cell Biology & Biotechnology, Tel Aviv University, Tel-Aviv, Israel
    For correspondence
    avigdor@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8485-9370
  4. Alan D Grossman

    Department of Biology, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    adg@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8235-7227

Funding

National Institute of General Medical Sciences (R01 GM050895; R35 GM122538)

  • Alan D Grossman

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

Copyright

© 2021, Jones 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. Joshua M Jones
  2. Ilana Grinberg
  3. Avigdor Eldar
  4. Alan D Grossman
(2021)
A mobile genetic element increases bacterial host fitness by manipulating development
eLife 10:e65924.
https://doi.org/10.7554/eLife.65924

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https://doi.org/10.7554/eLife.65924