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Energy source of flagellar type III secretion

Nature volume 451, pages 489–492 (2008)Cite this article

Abstract

Bacterial flagella contain a specialized secretion apparatus that functions to deliver the protein subunits that form the filament and other structures to outside the membrane1. This apparatus is related to the injectisome used by many gram-negative pathogens and symbionts to transfer effector proteins into host cells; in both systems this export mechanism is termed ‘type III’ secretion2,3. The flagellar secretion apparatus comprises a membrane-embedded complex of about five proteins, and soluble factors, which include export-dedicated chaperones and an ATPase, FliI, that was thought to provide the energy for export1,4. Here we show that flagellar secretion in Salmonella enterica requires the proton motive force (PMF) and does not require ATP hydrolysis by FliI. The export of several flagellar export substrates was prevented by treatment with the protonophore CCCP, with no accompanying decrease in cellular ATP levels. Weak swarming motility and rare flagella were observed in a mutant deleted for FliI and for the non-flagellar type-III secretion ATPases InvJ and SsaN. These findings show that the flagellar secretion apparatus functions as a proton-driven protein exporter and that ATP hydrolysis is not essential for type III secretion.

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Figure 1: Steps in flagellar assembly.
Figure 2: Inhibition of FlgM secretion by CCCP.
Figure 3: Effect of Δψ and ΔpH on FlgM export.
Figure 4: FliI is non-essential for flagellar assembly and function.

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Acknowledgements

We thank S. Williams for his help and permission for using the luminometer, F. Chevance for advice and assistance with strain constructions, M. Sarkar for assistance with MIC assays, and V. Clougherty for flagellar-staining experiments. M. Erhardt gratefully acknowledges scholarship support of the Studienstiftung des deutschen Volkes. This work was supported by Public Service grants (K.T.H. and D.F.B.) from the National Institutes of Health.

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Author notes

  1. Marc Erhardt

    Present address: Present address: Zentrum fur Molekulare Biologie Heidelberg, University of Heidelberg, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany.,

  2. Koushik Paul and Marc Erhardt: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112, USA,

    Koushik Paul, Marc Erhardt, Takanori Hirano, David F. Blair & Kelly T. Hughes

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  1. Koushik Paul
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  2. Marc Erhardt
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  3. Takanori Hirano
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Correspondence to David F. Blair or Kelly T. Hughes.

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Paul, K., Erhardt, M., Hirano, T. et al. Energy source of flagellar type III secretion. Nature 451, 489–492 (2008). https://doi.org/10.1038/nature06497

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