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. 2011 Jun 14;30(14):2972-81.
doi: 10.1038/emboj.2011.186.

Structural diversity of bacterial flagellar motors

Affiliations

Structural diversity of bacterial flagellar motors

Songye Chen et al. EMBO J. .

Abstract

The bacterial flagellum is one of nature's most amazing and well-studied nanomachines. Its cell-wall-anchored motor uses chemical energy to rotate a microns-long filament and propel the bacterium towards nutrients and away from toxins. While much is known about flagellar motors from certain model organisms, their diversity across the bacterial kingdom is less well characterized, allowing the occasional misrepresentation of the motor as an invariant, ideal machine. Here, we present an electron cryotomographical survey of flagellar motor architectures throughout the Bacteria. While a conserved structural core was observed in all 11 bacteria imaged, surprisingly novel and divergent structures as well as different symmetries were observed surrounding the core. Correlating the motor structures with the presence and absence of particular motor genes in each organism suggested the locations of five proteins involved in the export apparatus including FliI, whose position below the C-ring was confirmed by imaging a deletion strain. The combination of conserved and specially-adapted structures seen here sheds light on how this complex protein nanomachine has evolved to meet the needs of different species.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Flagellar motor structures obtained by ECT and subtomogram averaging. Left column: 20-nm thick central slices through tomograms of individual cells exhibiting flagellar motors, arranged in the same order as they appear on the phylogenetic tree shown in Supplementary Figure S2. Scale bar, 50 nm. Right column: Axial slices through average reconstructions of each motor. Scale bar, 10 nm. (Note that the motor structure of T. primitia was published previously; Murphy et al, 2006.)
Figure 2
Figure 2
Structure of the common core and its comparison with an earlier cryoEM single-particle reconstruction. Left: Isosurface of the S. enterica motor obtained by ECT and subtomogram averaging (red line) superimposed on an earlier single-particle reconstruction of purified basal bodies from the same organism (grey levels) (Thomas et al, 2006). Right: A generic motor structure obtained by aligning and averaging the axial slices of all 11 motors reconstructed here. Scale bar, 10 nm.
Figure 3
Figure 3
Assignment of densities. Manual segmentation of conserved (solid colours) and unconserved (dotted lines) motor components based on visual inspection. The conserved components from bottom to top are soluble export apparatus (FliH, FliI and FliJ); export platform and dome (FlhA, FlhB, FliO, FliP, FliQ and FliR); C-ring (FliG, FliM and FliN); MS-ring (FliF); stators (MotA and MotB in the H+-dependent stators or PomA and PomB in the Na+-dependent stators); rod (FliE, FlgB, FlgC, FlgF and FlgG); P-ring (FlgI); and L-ring (FlgH).
Figure 4
Figure 4
Structure of the export apparatus. (A) Enlarged view of the B. burgdorferi export apparatus and (B) 3D isosurface illustrating from top to bottom the export dome, torus and spherical density. (C) Atomic models of the cytoplasmic domains of FlhA above and the hexameric F1-ATPase, a homologue of FliI, shown at the same scale as (B) to show the correspondence of their sizes to the torus and spherical density. (D) Wild-type (top) and ΔfliI (bottom) C. jejuni motors confirming that the spherical density (red arrows, present above and absent below) is FliI.
Figure 5
Figure 5
Symmetries in the stator region. Upper row: Radial slices through the stator regions of three average motors before rotational averaging showing 16-, 16- and 13-fold symmetry, respectively. Lower row: Axial slices through the averaged and symmetrized motors with arrows showing the height at which the radial slices were taken. Scale bar, 10 nm.

References

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