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Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases

Nature Structural & Molecular Biology volume 18, pages 277–282 (2011)Cite this article

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Abstract

The proteins that form the bacterial flagellum are translocated to its distal end through the central channel of the growing flagellum by the flagellar-specific protein export apparatus, a family of the type III protein secretion system. FliI and FliJ are soluble components of this apparatus. FliI is an ATPase that has extensive structural similarity to the α and β subunits of FoF1-ATP synthase. FliJ is essential for export, but its function remains obscure. Here we show that the structure of FliJ derived from Salmonella enterica serovar Typhimurium is remarkably similar to that of the two-stranded α-helical coiled-coil part of the γ subunit of FoF1-ATP synthase and that FliJ promotes the formation of FliI hexamer rings by binding to the center of the ring. These results suggest that the type III protein export system and F- and V-type ATPases share a similar mechanism and an evolutionary relationship.

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Figure 1: Structure of FliJ.
Figure 2: Structural similarity between FliJ and the γ subunit of F1-ATPase.
Figure 3: Effect of FliJ on the formation of FliI rings.
Figure 4: Electron micrograph of the FliI–FliJ complex.
Figure 5: Comparison of the FliI and FliJ-FliI ring complexes.
Figure 6: Structure-based sequence alignment of FliI and the α and β subunits of F1-ATPase and pulldown assay to identify the FliI region that interacts with FliJ.
Figure 7: Schematic diagram showing a plausible model of the FliH–FliI–FliJ complex and its relative position and orientation to the export gate.

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Acknowledgements

We thank M. Shimada and K. Kazetani for technical assistance and N. Shimizu, M. Kawamoto and K. Hasegawa at SPring-8 for technical help in use of beamlines. T.I. is a research fellow of the Japan Society for the Promotion of Science. This work was supported in part by Grants-in-Aid for Scientific Research (18074006 to K.I., 22570161 to T. Minamino and 16087207 and 21227006 to K.N.) and the Targeted Proteins Research Program (TPRP) from the Ministry of Education, Science and Culture of Japan.

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Authors and Affiliations

  1. Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan

    Tatsuya Ibuki, Katsumi Imada, Tohru Minamino, Takayuki Kato, Tomoko Miyata & Keiichi Namba

  2. Department of Macromolecular Sciences, Graduate School of Sciences, Osaka University, Osaka, Japan

    Katsumi Imada

  3. Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency, Kawaguchi, Saitama, Japan

    Tohru Minamino

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  1. Tatsuya Ibuki
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Contributions

T.I. prepared samples and carried out crystallization and X-ray structure analysis. K.I. helped and supervised T.I. in X-ray crystallography. T. Minamino prepared protein expression constructs and carried out pulldown assays. T.K. helped and supervised T.I. in cryo-EM image analysis. T. Miyata collected cryo-EM images. K.N. supervised the whole project. T.I., K.I., T. Minamino and K.N. wrote the paper based on discussions with T.K. and T. Miyata.

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Correspondence to Katsumi Imada or Keiichi Namba.

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Ibuki, T., Imada, K., Minamino, T. et al. Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 18, 277–282 (2011). https://doi.org/10.1038/nsmb.1977

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