Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria
- Michigan State University, United States
- University of Michigan, United States
- National Institutes of Health, United States
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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-figure supplement 1 and Figure 2-figure supplement 1.
Article and author information
Author details
Anthony G Vecchiarelli
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
- Tâm Mignot, Aix Marseille University-CNRS UMR7283, France
Version history
- Received: July 2, 2018
- Accepted: November 19, 2018
- Accepted Manuscript published: December 6, 2018 (version 1)
- Version of Record published: January 10, 2019 (version 2)
- 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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Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria
eLife 7:e39723.
https://doi.org/10.7554/eLife.39723
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