1. Microbiology and Infectious Disease
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Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria

  1. Joshua S MacCready
  2. Pusparanee Hakim
  3. Eric J Young
  4. Longhua Hu
  5. Jian Liu
  6. Katherine W Osteryoung
  7. Anthony G Vecchiarelli  Is a corresponding author
  8. Daniel C Ducat  Is a corresponding author
  1. Michigan State University, United States
  2. University of Michigan, United States
  3. National Institutes of Health, United States
Research Article
  • Cited 27
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Cite this article as: eLife 2018;7:e39723 doi: 10.7554/eLife.39723

Abstract

Carboxysomes are protein-based bacterial organelles encapsulating key enzymes of the Calvin-Benson-Bassham cycle. Previous work has implicated a ParA-like protein (hereafter McdA) as important for spatially organizing carboxysomes along the longitudinal axis of the model cyanobacterium Synechococcus elongatus PCC 7942. Yet, how self-organization of McdA emerges and contributes to carboxysome positioning is unknown. Here, we identify a small protein, termed McdB that localizes to carboxysomes and drives emergent oscillatory patterning of McdA on the nucleoid. Our results demonstrate that McdB directly stimulates McdA ATPase activity and its release from DNA, driving carboxysome-dependent depletion of McdA locally on the nucleoid and promoting directed motion of carboxysomes towards increased concentrations of McdA. We propose that McdA and McdB are a previously unknown class of self-organizing proteins that utilize a Brownian-ratchet mechanism to position carboxysomes in cyanobacteria, rather than a cytoskeletal system. These results have broader implications for understanding spatial organization of protein mega-complexes and organelles in bacteria.

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Author details

  1. Joshua S MacCready

    Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Pusparanee Hakim

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Eric J Young

    Department of Biochemistry, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6770-6310

  4. Longhua Hu

    Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Jian Liu

    Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Katherine W Osteryoung

    Department of Plant Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Anthony G Vecchiarelli

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    For correspondence
    ave@umich.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6198-3245

  8. Daniel C Ducat

    Department of Biochemistry, Michigan State University, East Lansing, United States
    For correspondence
    ducatdan@msu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1520-0588

Funding

National Science Foundation (1517241)

  • Daniel C Ducat

Basic Energy Sciences (DE-FG02-91ER20021)

  • Daniel C Ducat

National Science Foundation (1817478)

  • Anthony G Vecchiarelli

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

Reviewing Editor

  1. Tâm Mignot, Aix Marseille University-CNRS UMR7283, France

Publication history

  1. Received: July 2, 2018
  2. Accepted: November 19, 2018
  3. Accepted Manuscript published: December 6, 2018 (version 1)
  4. Version of Record published: January 10, 2019 (version 2)
  5. Version of Record updated: February 12, 2019 (version 3)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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