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Journal of Bacteriology, June 2003, p. 3416-3428, Vol. 185, No. 11
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.11.3416-3428.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Type IV-Like Pili Formed by the Type II Secreton: Specificity, Composition, Bundling, Polar Localization, and Surface Presentation of Peptides

Guillaume Vignon,1 Rolf Köhler,1 Eric Larquet,2,{dagger} Stéphanie Giroux,3 Marie-Christine Prévost,3 Pascal Roux,4 and Anthony P. Pugsley1*

Unité de Génétique Moléculaire (CNRS URA 2172),1 Groupe de Microscopie Structurale Moléculaire (CNRS URA 2185),2 Plateau Technique de Microscopie Electronique,3 Centre d'Imagerie Dynamique, Institut Pasteur, Paris, France4

Received 14 January 2003/ Accepted 19 March 2003

The secreton or type II secretion machinery of gram-negative bacteria includes several type IV pilin-like proteins (the pseudopilins) that are absolutely required for secretion. We previously reported the presence of a bundled pilus composed of the pseudopilin PulG on the surface of agar-grown Escherichia coli K-12 cells expressing the Klebsiella oxytoca pullulanase (Pul) secreton genes at high levels (N. Sauvonnet, G. Vignon, A. P. Pugsley, and P. Gounon, EMBO J. 19:2221-2228, 2000). We show here that PulG is the only pseudopilin in purified pili and that the phenomenon is not restricted to the Pul secreton reconstituted in E. coli or to PulG. For example, high-level expression of the endogenous E. coli gsp secreton genes caused production of bundled pili composed of the pseudopilin GspG, and the Pul secreton was able to form pili composed of PulG-like proteins from secreton systems of other bacteria. PulG derivatives in which the C terminus was extended by the addition of eight different peptides were also assembled into pili and functioned in secretion. Three of the C-terminal peptides were shown to be exposed along the entire length of the assembled pili. Hence, the C terminus of PulG may represent a permissive site for the insertion of immunogenic epitopes or other peptide sequences. One of these PulG variants, with a six-histidine tag at its C terminus, formed nonpolar, nonbundled pili, suggesting that bundle formation and polar localization are not correlated with the ability of PulG to function in secretion. We propose that the PulG pilus is an artifactual manifestation of a periplasmic "pseudopilus" and that cycles of pseudopilus extension and retraction within the periplasm propel pullulanase through secretin channels in the outer membrane. Abnormally long pili that extend beyond the outer membrane are produced only when pilus length control and retraction are deregulated by overproduction of the major pseudopilus subunit (PulG).

* Corresponding author. Mailing address: Unité de Génétique Moléculaire, Institut Pasteur, 25, rue du Dr. Roux, 75724 Paris Cedex 15, France. Phone: 33/1-145688494. Fax: 33/0-145688960. E-mail: max{at}pasteur.fr.

{dagger} Present address: Laboratoire de Minéralogie-Cristallographie Paris, CNRS UMR 7590, Université Pierre et Marie Curie, 75252 Paris Cedex 05, France.

Journal of Bacteriology, June 2003, p. 3416-3428, Vol. 185, No. 11
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.11.3416-3428.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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