Previous Article | Next Article 
Journal of Bacteriology, April 2003, p. 2611-2617, Vol. 185, No. 8
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.8.2611-2617.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Three-Dimensional Structure of the Neisseria meningitidis Secretin PilQ Determined from Negative-Stain Transmission Electron Microscopy
Richard F. Collins,1 Robert C. Ford,1 Ashraf Kitmitto,1 Ranveig O. Olsen,2 Tone Tønjum,2 and Jeremy P. Derrick1*
Department of Biomolecular Sciences, UMIST, Manchester M60 1QD, United Kingdom,1
Centre for Molecular Biology and Neuroscience and Section of Molecular Microbiology, Institute of Microbiology, National Hospital, University of Oslo, N-0027 Oslo, Norway2
Received 21 October 2002/
Accepted 27 January 2003
The PilQ secretin from the pathogenic bacterium Neisseria meningitidis is an integral outer membrane protein complex which plays a crucial role in the biogenesis of type IV pili. We present here the first three-dimensional structure of this type of secretin at 2.5-nm resolution, obtained by single-particle averaging methods applied to the purified protein complex visualized in a negative stain. In projection, the PilQ complex is circular, with a donut-like appearance. When viewed from the side it has a rounded, conical profile. The complex was demonstrated to have 12-fold rotational symmetry, and this property was used to improve the quality of the density map by symmetry averaging. The dominant feature of the structure is a cavity, 10 nm deep, within the center of the molecule. The cavity is funnel-shaped in cross section, measures 6.5 nm in diameter at the top of the complex, and tapers to a closed point, effectively blocking formation of a continuous pore through the PilQ complex. These results suggest that the complex would have to undergo a conformational change in order to accommodate an assembled pilus fiber of diameter 6.5 nm running through the outer membrane.
* Corresponding author. Mailing address: Department of Biomolecular Sciences, UMIST, P.O. Box 88, Manchester M60 1QD, United Kingdom. Phone: 44-0161-200-4207. Fax: 44-0161-236-0409. E-mail:
Jeremy.Derrick{at}umist.ac.uk.
Journal of Bacteriology, April 2003, p. 2611-2617, Vol. 185, No. 8
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.8.2611-2617.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Collins, R. F., Saleem, M., Derrick, J. P.
(2007). Purification and Three-Dimensional Electron Microscopy Structure of the Neisseria meningitidis Type IV Pilus Biogenesis Protein PilG. J. Bacteriol.
189: 6389-6396
[Abstract]
[Full Text]
-
Balasingham, S. V., Collins, R. F., Assalkhou, R., Homberset, H., Frye, S. A., Derrick, J. P., Tonjum, T.
(2007). Interactions between the Lipoprotein PilP and the Secretin PilQ in Neisseria meningitidis. J. Bacteriol.
189: 5716-5727
[Abstract]
[Full Text]
-
Assalkhou, R., Balasingham, S., Collins, R. F., Frye, S. A., Davidsen, T., Benam, A. V., Bjoras, M., Derrick, J. P., Tonjum, T.
(2007). The outer membrane secretin PilQ from Neisseria meningitidis binds DNA. Microbiology
153: 1593-1603
[Abstract]
[Full Text]
-
Helm, R. A., Barnhart, M. M., Seifert, H. S.
(2007). pilQ Missense Mutations Have Diverse Effects on PilQ Multimer Formation, Piliation, and Pilus Function in Neisseria gonorrhoeae. J. Bacteriol.
189: 3198-3207
[Abstract]
[Full Text]
-
Frye, S. A., Assalkhou, R., Collins, R. F., Ford, R. C., Petersson, C., Derrick, J. P., Tonjum, T.
(2006). Topology of the outer-membrane secretin PilQ from Neisseria meningitidis. Microbiology
152: 3751-3764
[Abstract]
[Full Text]
-
Chami, M., Guilvout, I., Gregorini, M., Remigy, H. W., Muller, S. A., Valerio, M., Engel, A., Pugsley, A. P., Bayan, N.
(2005). Structural Insights into the Secretin PulD and Its Trypsin-resistant Core. J. Biol. Chem.
280: 37732-37741
[Abstract]
[Full Text]
-
Rasmussen, A. W., Alexander, H. L., Perkins-Balding, D., Shafer, W. M., Stojiljkovic, I.
(2005). Resistance of Neisseria meningitidis to the Toxic Effects of Heme Iron and Other Hydrophobic Agents Requires Expression of ght. J. Bacteriol.
187: 5214-5223
[Abstract]
[Full Text]
-
Collins, R. F., Frye, S. A., Balasingham, S., Ford, R. C., Tonjum, T., Derrick, J. P.
(2005). Interaction with Type IV Pili Induces Structural Changes in the Bacterial Outer Membrane Secretin PilQ. J. Biol. Chem.
280: 18923-18930
[Abstract]
[Full Text]
-
Bose, N., Taylor, R. K.
(2005). Identification of a TcpC-TcpQ Outer Membrane Complex Involved in the Biogenesis of the Toxin-Coregulated Pilus of Vibrio cholerae. J. Bacteriol.
187: 2225-2232
[Abstract]
[Full Text]
-
Collins, R. F., Frye, S. A., Kitmitto, A., Ford, R. C., Tonjum, T., Derrick, J. P.
(2004). Structure of the Neisseria meningitidis Outer Membrane PilQ Secretin Complex at 12 A Resolution. J. Biol. Chem.
279: 39750-39756
[Abstract]
[Full Text]
-
Maier, B., Koomey, M., Sheetz, M. P.
(2004). A force-dependent switch reverses type IV pilus retraction. Proc. Natl. Acad. Sci. USA
101: 10961-10966
[Abstract]
[Full Text]
-
Burghout, P., van Boxtel, R., Van Gelder, P., Ringler, P., Muller, S. A., Tommassen, J., Koster, M.
(2004). Structure and Electrophysiological Properties of the YscC Secretin from the Type III Secretion System of Yersinia enterocolitica. J. Bacteriol.
186: 4645-4654
[Abstract]
[Full Text]
-
Gil, H., Benach, J. L., Thanassi, D. G.
(2004). Presence of Pili on the Surface of Francisella tularensis. Infect. Immun.
72: 3042-3047
[Abstract]
[Full Text]
-
Chen, C.-j., Tobiason, D. M., Thomas, C. E., Shafer, W. M., Seifert, H. S., Sparling, P. F.
(2004). A Mutant Form of the Neisseria gonorrhoeae Pilus Secretin Protein PilQ Allows Increased Entry of Heme and Antimicrobial Compounds. J. Bacteriol.
186: 730-739
[Abstract]
[Full Text]
-
Nesper, J., Hill, C. M. D., Paiment, A., Harauz, G., Beis, K., Naismith, J. H., Whitfield, C.
(2003). Translocation of Group 1 Capsular Polysaccharide in Escherichia coli Serotype K30: STRUCTURAL AND FUNCTIONAL ANALYSIS OF THE OUTER MEMBRANE LIPOPROTEIN Wza. J. Biol. Chem.
278: 49763-49772
[Abstract]
[Full Text]
-
Nikaido, H.
(2003). Molecular Basis of Bacterial Outer Membrane Permeability Revisited. Microbiol. Mol. Biol. Rev.
67: 593-656
[Abstract]
[Full Text]
-
Peabody, C. R., Chung, Y. J., Yen, M.-R., Vidal-Ingigliardi, D., Pugsley, A. P., Saier, M. H. Jr
(2003). Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology
149: 3051-3072
[Abstract]
[Full Text]