The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type
- California Institute of Technology, United States
- University of Southern California, United States
Abstract
The bacterial flagellar motor, a cell-envelope-embedded macromolecular machine that functions as a cellular propeller, exhibits significant structural variability between species. Different torque-generating stator modules allow motors to operate in different pH, salt or viscosity levels. How such diversity evolved is unknown. Here we use electron cryo-tomography to determine the in situ macromolecular structures of three Gammaproteobacteria motors: Legionella pneumophila, Pseudomonas aeruginosa, and Shewanella oneidensis, providing the first views of intact motors with dual stator systems. Complementing our imaging with bioinformatics analysis, we find a correlation between the motor's stator system and its structural elaboration. Motors with a single H+-driven stator have only the core periplasmic P- and L-rings; those with dual H+-driven stators have an elaborated P-ring; and motors with Na+ or Na+/H+-driven stators have both their P- and L-rings embellished. Our results suggest an evolution of structural elaboration that may have enabled pathogenic bacteria to colonize higher-viscosity environments in animal hosts.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.The ECT structures have been deposited in the EMDB under the following accession numbers, EMD-0464 for Legionella pneumophila motor, EMD-0465 for Pseudomonas aeruginosa motor and EMD-0467 for Shewanella oneidensis MR-1 motor
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Shewanella oneidensis MR-1 motorEM Data Bank, EMD-0467.
Article and author information
Author details
Funding
National Institutes of Health (R01 AI127401)
- Mohammed Kaplan
- Debnath Ghosal
- Poorna Subramanian
- Catherine M Oikonomou
- Andreas Kjaer
- Davi R Ortega
- Ariane Briegel
- Grant J Jensen
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Rubicon fellowship)
- Mohammed Kaplan
Air Force Office of Scientific Research
- Sahand Pirbadian
Air Force Office of Scientific Research (FA955014-1-0294)
- Mohamed Y El-Naggar
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Edward H Egelman, University of Virginia, United States
Version history
- Received: November 8, 2018
- Accepted: December 19, 2018
- Accepted Manuscript published: January 16, 2019 (version 1)
- Version of Record published: February 14, 2019 (version 2)
Copyright
© 2019, Kaplan 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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The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type
eLife 8:e43487.
https://doi.org/10.7554/eLife.43487
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