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.
Highlights
The bacterial flagellum is a macromolecular machine that transforms the movement of ions (H+, Na+ or other cations) across the cell membrane into a mechanical torque to move the bacterial cell through its environment (Ito and Takahashi, 2017; Sowa and Berry, 2008)
While the S. oneidensis and P. aeruginosa averages showed clear densities corresponding to the stators (Figure 1E,F,K and L, dark orange density), none were visible in the L. pneumophila average, suggesting that they were more variable, or dynamic and are not visible in the average (see e.g., (Chen et al, 2011; Zhu et al, 2017))
We find that motors with dual H+-driven stator systems represent a hybrid structure between the two, elaborating their P-rings with one of the five components of the T- and H-rings, MotY
Summary
The bacterial flagellum is a macromolecular machine that transforms the movement of ions (H+, Na+ or other cations) across the cell membrane into a mechanical torque to move the bacterial cell through its environment (Ito and Takahashi, 2017; Sowa and Berry, 2008). The flagellum consists of a cell-envelope-embedded motor, a hook which acts as a universal joint and a long propeller-like filament (Berg, 2003; Erhardt et al, 2010). Flagella can exhibit a more complex behavior; it was recently reported that the Shewanella putrefaciens flagellum can wrap around the cell to mediate a screw-like motion that allows the cell to escape narrow traps (Kuhn et al, 2017). Besides their role in motility, bacterial flagella participate in other vital activities of the cell such as biofilm formation (Belas, 2014).
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