PomX, a ParA/MinD ATPase activating protein, is a triple regulator of cell division in Myxococcus xanthus

  1. Dominik Schumacher
  2. Andrea Harms
  3. Silke Bergeler
  4. Erwin Frey
  5. Lotte Sogaard-Andersen  Is a corresponding author
  1. Max Planck Institute for Terrestrial Microbiology, Germany
  2. Ludwig-Maximilians-Universität München, Germany

Abstract

Cell division site positioning is precisely regulated but the underlying mechanisms are incompletely understood. In the social bacterium Myxococcus xanthus, the ~15 MDa tripartite PomX/Y/Z complex associates with and translocates across the nucleoid in a PomZ ATPase-dependent manner to directly position and stimulate formation of the cytokinetic FtsZ-ring at midcell, and then undergoes fission during division. Here, we demonstrate that PomX consists of two functionally distinct domains and has three functions. The N-terminal domain stimulates ATPase activity of the ParA/MinD ATPase PomZ. The C-terminal domain interacts with PomY and forms polymers, which serve as a scaffold for PomX/Y/Z complex formation. Moreover, the PomX/PomZ interaction is important for fission of the PomX/Y/Z complex. These observations together with previous work support that the architecturally diverse ATPase activating proteins of ParA/MinD ATPases are highly modular and use the same mechanism to activate their cognate ATPase via a short positively charged N-terminal extension.

Data availability

All data supporting this study are available within the article and supporting files. Source data files have been provided for Figures 1, 2, 3, 4, 5 and 6.

Article and author information

Author details

  1. Dominik Schumacher

    Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Andrea Harms

    Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Silke Bergeler

    Arnold Sommerfeld Center for Theoretical Physics, Ludwig-Maximilians-Universität München, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Erwin Frey

    Arnold Sommerfeld Center for Theoretical Physics, Ludwig-Maximilians-Universität München, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8792-3358
  5. Lotte Sogaard-Andersen

    Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    For correspondence
    sogaard@mpi-marburg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0674-0013

Funding

Deutsche Forschungsgemeinschaft (TRR 174)

  • Erwin Frey
  • Lotte Sogaard-Andersen

Max Planck Gesellschaft (NA)

  • Lotte Sogaard-Andersen

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

Reviewing Editor

  1. Gisela Storz, National Institute of Child Health and Human Development, United States

Version history

  1. Received: December 30, 2020
  2. Accepted: March 17, 2021
  3. Accepted Manuscript published: March 18, 2021 (version 1)
  4. Version of Record published: March 24, 2021 (version 2)

Copyright

© 2021, Schumacher 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.

Metrics

  • 1,191
    Page views
  • 196
    Downloads
  • 4
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Dominik Schumacher
  2. Andrea Harms
  3. Silke Bergeler
  4. Erwin Frey
  5. Lotte Sogaard-Andersen
(2021)
PomX, a ParA/MinD ATPase activating protein, is a triple regulator of cell division in Myxococcus xanthus
eLife 10:e66160.
https://doi.org/10.7554/eLife.66160

Share this article

https://doi.org/10.7554/eLife.66160

Further reading

    1. Cell Biology
    2. Neuroscience
    Haibin Yu, Dandan Liu ... Kai Yuan
    Research Article

    O-GlcNAcylation is a dynamic post-translational modification that diversifies the proteome. Its dysregulation is associated with neurological disorders that impair cognitive function, and yet identification of phenotype-relevant candidate substrates in a brain-region specific manner remains unfeasible. By combining an O-GlcNAc binding activity derived from Clostridium perfringens OGA (CpOGA) with TurboID proximity labeling in Drosophila, we developed an O-GlcNAcylation profiling tool that translates O-GlcNAc modification into biotin conjugation for tissue-specific candidate substrates enrichment. We mapped the O-GlcNAc interactome in major brain regions of Drosophila and found that components of the translational machinery, particularly ribosomal subunits, were abundantly O-GlcNAcylated in the mushroom body of Drosophila brain. Hypo-O-GlcNAcylation induced by ectopic expression of active CpOGA in the mushroom body decreased local translational activity, leading to olfactory learning deficits that could be rescued by dMyc overexpression-induced increase of protein synthesis. Our study provides a useful tool for future dissection of tissue-specific functions of O-GlcNAcylation in Drosophila, and suggests a possibility that O-GlcNAcylation impacts cognitive function via regulating regional translational activity in the brain.

    1. Cancer Biology
    2. Cell Biology
    Ibtisam Ibtisam, Alexei F Kisselev
    Short Report

    Rapid recovery of proteasome activity may contribute to intrinsic and acquired resistance to FDA-approved proteasome inhibitors. Previous studies have demonstrated that the expression of proteasome genes in cells treated with sub-lethal concentrations of proteasome inhibitors is upregulated by the transcription factor Nrf1 (NFE2L1), which is activated by a DDI2 protease. Here, we demonstrate that the recovery of proteasome activity is DDI2-independent and occurs before transcription of proteasomal genes is upregulated but requires protein translation. Thus, mammalian cells possess an additional DDI2 and transcription-independent pathway for the rapid recovery of proteasome activity after proteasome inhibition.