The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type
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.
Additional Information
© 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. Received: November 8, 2018; Accepted: December 19, 2018; Accepted Manuscript published: January 16, 2019 (version 1). We thank Dr. Songye Chen for technical support. This work is supported by the National Institutes of Health (NIH, grant R01 AI127401 to G.J.J.). M.K. is supported by a postdoctoral Rubicon fellowship from De Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO). S.P. and M.Y.E.-N. are supported by the Air Force Office of Scientific Research Presidential Early Career Award for Scientists and Engineers (FA955014-1-0294, to M.Y.E.-N.). 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 motorAttached Files
Published - elife-43487-v2.pdf
Supplemental Material - elife-43487-supp1-v2.docx
Supplemental Material - elife-43487-supp2-v2.docx
Supplemental Material - elife-43487-supp3-v2.docx
Supplemental Material - elife-43487-transrepform-v2.docx
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Additional details
- PMCID
- PMC6375700
- Eprint ID
- 92398
- Resolver ID
- CaltechAUTHORS:20190122-131221284
- NIH
- R01 AI127401
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)
- Air Force Office of Scientific Research (AFOSR)
- FA955014-1-0294
- Created
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2019-01-22Created from EPrint's datestamp field
- Updated
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2021-11-16Created from EPrint's last_modified field