CaltechAUTHORS
  A Caltech Library Service

The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type

Kaplan, Mohammed and Ghosal, Debnath and Subramanian, Poorna and Oikonomou, Catherine M. and Kjær, Andreas and Pirbadian, Sahand and Ortega, Davi R. and Briegel, Ariane and El-Naggar, Mohamed Y. and Jensen, Grant J. (2019) The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type. eLife, 8 . Art. No. e43487. ISSN 2050-084X. PMCID PMC6375700. http://resolver.caltech.edu/CaltechAUTHORS:20190122-131221284

[img] PDF - Published Version
Creative Commons Attribution.

2042Kb
[img] MS Word (Raw T- and H-rings proteins Blast results for all species in Tables 1–4) - Supplemental Material
Creative Commons Attribution.

19Kb
[img] MS Word (Raw stator proteins Blast results for all species in Tables 1–4) - Supplemental Material
Creative Commons Attribution.

23Kb
[img] MS Word (S. oneidensis strains used in this study) - Supplemental Material
Creative Commons Attribution.

13Kb
[img] MS Word (Transparent reporting form) - Supplemental Material
Creative Commons Attribution.

244Kb

Use this Persistent URL to link to this item: http://resolver.caltech.edu/CaltechAUTHORS:20190122-131221284

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.43487DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6375700/PubMed CentralArticle
ORCID:
AuthorORCID
Kjær, Andreas0000-0002-0096-5764
Ortega, Davi R.0000-0002-8344-2335
Briegel, Ariane0000-0003-3733-3725
Jensen, Grant J.0000-0003-1556-4864
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 motor
Funders:
Funding AgencyGrant Number
NIHR01 AI127401
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)UNSPECIFIED
Air Force Office of Scientific Research (AFOSR)FA955014-1-0294
PubMed Central ID:PMC6375700
Record Number:CaltechAUTHORS:20190122-131221284
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190122-131221284
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92398
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:22 Jan 2019 21:51
Last Modified:21 Mar 2019 23:00

Repository Staff Only: item control page