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: <i>Legionella pneumophila</i>, <i>Pseudomonas aeruginosa</i>, and <i>Shewanella oneidensis</i>, 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.