Distinct architectural requirements for the parS centromeric sequence of the pSM19035 plasmid partition machinery

  1. Andrea Volante
  2. Juan Carlos Alonso
  3. Kiyoshi Mizuuchi  Is a corresponding author
  1. National Institute of Diabetes and Digestive and Kidney Diseases, United States
  2. National Center for Biotechnology, Spain

Abstract

Three-component ParABS partition systems ensure stable inheritance of many bacterial chromosomes and low-copy-number plasmids. ParA localizes to the nucleoid through its ATP-dependent non-specific DNA binding activity, whereas centromere-like parS-DNA and ParB form partition complexes that activate ParA-ATPase to drive the system dynamics. The essential parS sequence arrangements vary among ParABS systems, reflecting the architectural diversity of their partition complexes. Here, we focus on the pSM19035 plasmid partition system that uses a ParBpSM of the ribbon-helix-helix (RHH) family. We show that parSpSM with four or more contiguous ParBpSM-binding sequence repeats is required to assemble a stable ParApSM-ParBpSM complex and efficiently activate the ParApSM-ATPase, stimulating complex disassembly. Disruption of the contiguity of the parSpSM sequence array destabilizes the ParApSM-ParBpSM complex and prevents efficient ATPase activation. Our findings reveal the unique architecture of the pSM19035 partition complex and how it interacts with nucleoid-bound ParApSM-ATP.

Data availability

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

Article and author information

Author details

  1. Andrea Volante

    National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Juan Carlos Alonso

    Department of Microbial Biotechnology, National Center for Biotechnology, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5178-7179
  3. Kiyoshi Mizuuchi

    National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, United States
    For correspondence
    kiyoshimi@niddk.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8193-9244

Funding

National Institute of Diabetes and Digestive and Kidney Diseases

  • Kiyoshi Mizuuchi

Ministerio de Ciencia e Innovación (2018-097054-B-I00,2021AEP031)

  • Juan Carlos Alonso

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

Reviewing Editor

  1. Jie Xiao, Johns Hopkins University, United States

Version history

  1. Received: April 14, 2022
  2. Preprint posted: May 30, 2022 (view preprint)
  3. Accepted: September 2, 2022
  4. Accepted Manuscript published: September 5, 2022 (version 1)
  5. Version of Record published: September 22, 2022 (version 2)
  6. Version of Record updated: September 23, 2022 (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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  1. Andrea Volante
  2. Juan Carlos Alonso
  3. Kiyoshi Mizuuchi
(2022)
Distinct architectural requirements for the parS centromeric sequence of the pSM19035 plasmid partition machinery
eLife 11:e79480.
https://doi.org/10.7554/eLife.79480

Share this article

https://doi.org/10.7554/eLife.79480

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