Functional Regulators of Bacterial Flagella

Abstract

Bacteria move by a variety of mechanisms, but the best understood types of motility are powered by flagella (72). Flagella are complex machines embedded in the cell envelope that rotate a long extracellular helical filament like a propeller to push cells through the environment. The flagellum is one of relatively few biological machines that experience continuous 360° rotation, and it is driven by one of the most powerful motors, relative to its size, on earth. The rotational force (torque) generated at the base of the flagellum is essential for motility, niche colonization, and pathogenesis. This review describes regulatory proteins that control motility at the level of torque generation.

Keywords: EpsE; FliG; MotA; YcgR; biofilm; swarming.

Figure legend 1:. Models of flagellar structure and torque generation.

Panel A) Cross-section cartoon of the Gram-negative flagellum that highlights major architectural domains. OM – outer membrane, PG – peptidoglycan, PM – plasma membrane. The flagellar filament (colored green) is truncated as drawn; the entire filament is helical in structure and can extend for multiple cell lengths. The stator units (colored brown) are discrete complexes separate from the flagellar structure. They can range in number up to 11 surrounding an E. coli flagellum. Panel B) Stator-rotor interaction provides torque for rotation. The relative location of the protonatable Asp32 residue that serves as the conduit for proton motive force consumption is indicated in red based on reference 26. The stator complex sits atop the gear-like rotor made of FliG and likely generates force when MotA makes a piston-like conformational change. Panel C) Stator complexes change conformation upon interaction with the flagellum. Panel reprinted with permission from reference .

Figure legend 2:. Motor resurrection.

Panel A) A motor resurrection experiment reprinted with permission from reference 18. The X-axis is time following stator gene induction, the Y-axis is the rotation speed of a tethered cell, and the dots are instantaneous rotation speeds. Panel B) Freeze-fracture electron microscopy of membranes containing flagellar basal bodies and stator units, reprinted and modified with permission from reference 80. The left panel is a membrane from wild-type cells, and the right panel is a membrane from a mot mutant. Annotation and white circle added to figure. The circles surround a single flagellar basal body and either include the densities attributed to stator units (left) or emphasize their absence (right).

Figure legend 3:. Ultrastructure of the flagellar basal body and C-ring.

A three-dimensional reconstruction of an electron micrograph of purified flagella. Densities attributed to the flagellar basal body (yellow), rotor (red), and the rest of the C-ring (blue) are indicated. Stator complexes (purple) were added to show their likely position, even though they were not included in the actual data set. Reprinted with permission from reference .

Figure legend 4:

Models for functional regulators of the bacterial flagellum. PG – peptidoglycan. PM – plasma membrane. Basal body (purple), rotor/C-ring (pink), stator units (brown), functional regulator (unique color). EpsE (B. subtilis, red) binds to the rotor and disconnects it from the stators. MotI bound to c-di-GMP (B. subtilis, blue) binds to the stator units and disconnects them from the rotor. FlgZ bound to c-di-GMP (P. aeruginosa, green) binds to one set of stators (MotCD) and disconnects them from the rotor while permitting another set (MotAB) to associate. Phosphorylated CheY (R. sphaeroides, yellow) interacts with the C-ring and increases rotor interaction with the stator units. YcgR bound to c-di-GMP (E. coli, orange) binds to stators units and the rotor simultaneously to reduce rotation speeds and bias rotation in the counterclockwise direction. FliL (magenta) increases torque likely by relieving inhibition of proton flow through the stator by the MotB plug domain. SwrD (B. subtilis, lavender) increases torque, perhaps by stabilizing stators at the rotor, but the mechanism and the location of SwrD are unknown.