Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching

Abstract

Rotation of the bacterial flagellar filament is responsible for bacterial motility. The direction of rotation determines whether the bacteria run smoothly forward or tumble to change their trajectory. The flagellar motor drives this rotation either clockwise or counter-clockwise, with the direction regulated by the flagellar switch complex. One of its components, a ring-shaped protein called FliG, applies the twisting motion or torque that enables the motor to switch direction — a notable feat since the flagellum rotates at hundreds of revolutions per second, yet reverses direction in less than a millisecond. The full-length structure of FliG has now been determined, and the conformational changes that are involved in switching between the direction of rotation identified. The bacterial flagellar motor drives the rotation of flagellar filaments, propelling bacteria through viscous media. The rotation can switch from an anticlockwise to a clockwise direction, determining a smooth or tumbling motion. A protein called FliG forms a ring in the motor's rotor, and has been proposed to adopt distinct conformations that induce switching. Here, the full-length structure of FliG is presented, and conformational changes are identified that are involved in switching between clockwise and anticlockwise rotations. The flagellar motor drives the rotation of flagellar filaments at hundreds of revolutions per second1,2, efficiently propelling bacteria through viscous media3. The motor uses the potential energy from an electrochemical gradient of cations4,5 across the cytoplasmic membrane to generate torque. A rapid switch from anticlockwise to clockwise rotation determines whether a bacterium runs smoothly forward or tumbles to change its trajectory6,7. A protein called FliG forms a ring in the rotor of the flagellar motor that is involved in the generation of torque8,9,10,11,12,13 through an interaction with the cation-channel-forming stator subunit MotA12. FliG has been suggested to adopt distinct conformations that induce switching but these structural changes and the molecular mechanism of switching are unknown. Here we report the molecular structure of the full-length FliG protein, identify conformational changes that are involved in rotational switching and uncover the structural basis for the formation of the FliG torque ring. This allows us to propose a model of the complete ring and switching mechanism in which conformational changes in FliG reverse the electrostatic charges involved in torque generation.