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Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism

Abstract

The bacterial flagellum is a motile organelle, and the flagellar hook is a short, highly curved tubular structure that connects the flagellar motor to the long filament acting as a helical propeller. The hook is made of about 120 copies of a single protein, FlgE, and its function as a nano-sized universal joint is essential for dynamic and efficient bacterial motility and taxis. It transmits the motor torque to the helical propeller over a wide range of its orientation for swimming and tumbling. Here we report a partial atomic model of the hook obtained by X-ray crystallography of FlgE31, a major proteolytic fragment of FlgE lacking unfolded terminal regions, and by electron cryomicroscopy and three-dimensional helical image reconstruction of the hook. The model reveals the intricate molecular interactions and a plausible switching mechanism for the hook to be flexible in bending but rigid against twisting for its universal joint function.

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Acknowledgements

We thank R. M. Macnab, who passed away suddenly in September 2003, for his invaluable discussion on the structure and function of the flagellar hook; the staff members of beamline ID29 at the European Synchrotron Radiation Facility (ESRF) in Grenoble and beamline BL41XU at the 8 GeV Super Photon ring (SPring-8) in Harima for their help for the data collection; and F. Oosawa and S. Asakura for continuous support and encouragement.

Author information

Correspondence to Keiichi Namba.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Table 1

Regions involved in intersubunit interactions, listing amino acid residues of FlgE31 involved in the interactions along the 11-start, 5-start and 6-start directions of the hook structure. (DOC 35 kb)

Supplementary Table 2

Summary of refinement statistics of the X-ray crystal structure analysis of FlgE31. (DOC 41 kb)

Supplementary Video 1

Rolling rotation (or “smoke-ring” rotation) of an atomic model of coiled hook during its function as a universal joint. The atomic model is the one shown in Figure 5. During the rolling rotation, each protofilament goes through extension and compression with every revolution. (MOV 13182 kb)

Supplementary Video 2

Possible conformational changes of the protofilaments and subunits on the longitudinal section of the tube wall of the coiled hook during its rolling rotation (four protofilaments have been removed). The inner surface of the layer made of D1 domains can also be seen. (MOV 11056 kb)

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Further reading

Figure 1: Stereo view of the Cα backbone trace of FlgE31.
Figure 2: Docking of the atomic model of FlgE31 into the outer two domains of the hook.
Figure 3: Stereo view of the atomic model of the D1–D2 part of the straight hook.
Figure 4: Magnified views of intermolecular interactions along various helical lines of the straight hook.
Figure 5: Atomic model of the supercoiled hook.
Figure 6: Simulated extension and compression of hook protofilament.

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