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The structural complexity of the Gammaproteobacteria flagellar motor is related to the type of its torque-generating stators

Kaplan, Mohammed and Ghosal, Debnath and Subramanian, Poorna and Oikonomou, Catherine M. and Kjær, Andreas and Pirbadian, Sahand and Ortega, Davi R. and El-Naggar, Mohamed Y. and Jensen, Grant J. (2018) The structural complexity of the Gammaproteobacteria flagellar motor is related to the type of its torque-generating stators. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20181008-162019924

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Abstract

The bacterial flagellar motor is a cell-envelope-embedded macromolecular machine that functions as a propeller to move the cell. Rather than being an invariant machine, the flagellar motor exhibits significant variability between species, allowing bacteria to adapt to, and thrive in, a wide range of environments. For instance, different torque- generating stator modules allow motors to operate in conditions with different pH and sodium concentrations and some motors are adapted to drive motility in high-viscosity environments. How such diversity evolved is unknown. Here we use electron cryo-tomography to determine the in situ macromolecular structures of the flagellar motors of three Gammaproteobacteria species: Legionella pneumophila, Pseudomonas aeruginosa, and Shewanella oneidensis MR-1, providing the first views of intact motors with dual stator systems. Complementing our imaging with bioinformatics analysis, we find a correlation between the stator system of the motor and its structural complexity. Motors with a single H+-driven stator system have only the core P- and L-rings in their periplasm; those with dual H+-driven stator systems have an extra component elaborating their P-ring; and motors with Na+- (or dual Na+-H+)- driven stator systems have additional rings surrounding both their P- and L-rings. Our results suggest an evolution of structural complexity that may have enabled pathogenic bacteria like L. pneumophila and P. aeruginosa to colonize higher-viscosity environments in animal hosts.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/369397DOIDiscussion Paper
ORCID:
AuthorORCID
Kaplan, Mohammed0000-0002-0759-0459
Ghosal, Debnath0000-0002-2227-0330
Oikonomou, Catherine M.0000-0003-2312-4746
Kjær, Andreas0000-0002-0096-5764
Ortega, Davi R.0000-0002-8344-2335
Jensen, Grant J.0000-0003-1556-4864
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. 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.).
Funders:
Funding AgencyGrant Number
NIHR01 AI127401
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)UNSPECIFIED
Air Force Office of Scientific Research (AFOSR)FA955014-1-0294
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Record Number:CaltechAUTHORS:20181008-162019924
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181008-162019924
Official Citation:The structural complexity of the Gammaproteobacteria flagellar motor is related to the type of its torque-generating stators Mohammed Kaplan, Debnath Ghosal, Poorna Subramanian, Catherine M Oikonomou, Andreas Kjaer, Sahand Pirbadian, Davi R Ortega, Mohamed Y El-Naggar, Grant J Jensen bioRxiv 369397; doi: https://doi.org/10.1101/369397
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90171
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:09 Oct 2018 14:53
Last Modified:03 Oct 2019 20:22

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