Structural basis of directional switching by the bacterial flagellum

• Published in: Nature microbiology Vol. 9; no. 5; pp. 1282 - 1292
• Main Authors: Johnson, Steven, Deme, Justin C., Furlong, Emily J., Caesar, Joseph J. E., Chevance, Fabienne F. V., Hughes, Kelly T., Lea, Susan M.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.05.2024; Nature Publishing Group
• Subjects: 101/28; 631/326/88; 631/45/535/1258/1259; 82/80; 82/83; Bacteria; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Basal bodies; Basal Bodies - chemistry; Basal Bodies - metabolism; Biomedical and Life Sciences; Chemotactic response; Cryoelectron Microscopy; Electron microscopes; Flagella; Flagella - chemistry; Flagella - metabolism; Flagella - ultrastructure; FliG protein; Infectious Diseases; Life Sciences; Medical Microbiology; Microbiology; Microscopy; Models, Molecular; Parasitology; Protein Conformation; Rotation; Salmonella; Salmonella - chemistry; Salmonella - metabolism; Salmonella typhimurium - chemistry; Salmonella typhimurium - metabolism; Virology
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-024-01630-z

The bacterial flagellum is a macromolecular protein complex that harvests energy from uni-directional ion flow across the inner membrane to power bacterial swimming via rotation of the flagellar filament. Rotation is bi-directional, with binding of a cytoplasmic chemotactic response regulator controlling reversal, though the structural and mechanistic bases for rotational switching are not well understood. Here we present cryoelectron microscopy structures of intact Salmonella flagellar basal bodies (3.2–5.5 Å), including the cytoplasmic C-ring complexes required for power transmission, in both counter-clockwise and clockwise rotational conformations. These reveal 180° movements of both the N- and C-terminal domains of the FliG protein, which, when combined with a high-resolution cryoelectron microscopy structure of the MotA 5 B 2 stator, show that the stator shifts from the outside to the inside of the C-ring. This enables rotational switching and reveals how uni-directional ion flow across the inner membrane is used to accomplish bi-directional rotation of the flagellum. Cryoelectron microscopy analyses of the counter-clockwise and clockwise states of the Salmonella Typhimurium C-ring reveal the structural bases for changes in rotation of the bacterial flagellum.