Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis

Type IV pili are polymeric fibers which protrude from the cell surface and play a critical role in adhesion and invasion by pathogenic bacteria. The secretion of pili across the periplasm and outer membrane is mediated by a specialized secretin protein, PilQ, but the way in which this large channel...

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Bibliographic Details
Published in:	PLoS pathogens Vol. 8; no. 9; p. e1002923
Main Authors:	Berry, Jamie-Lee, Phelan, Marie M, Collins, Richard F, Adomavicius, Tomas, Tønjum, Tone, Frye, Stefan A, Bird, Louise, Owens, Ray, Ford, Robert C, Lian, Lu-Yun, Derrick, Jeremy P
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 01-09-2012 Public Library of Science (PLoS)
Subjects:	Bacterial Adhesion Bacterial Outer Membrane Proteins - chemistry Bacterial Outer Membrane Proteins - metabolism Bacteriology Biology Cell Membrane - metabolism Fimbriae Proteins - chemistry Fimbriae Proteins - metabolism Fimbriae, Bacterial - metabolism Fimbriae, Bacterial - ultrastructure Health aspects Meningitis Microbiology Models, Molecular Neisseria meningitidis Neisseria meningitidis - metabolism Neisseria meningitidis - ultrastructure Nuclear Magnetic Resonance, Biomolecular Periplasm - metabolism Physiological aspects Protein Binding Protein Folding Protein Structure, Tertiary Proteins Virulence (Microbiology) United Kingdom
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Summary:	Type IV pili are polymeric fibers which protrude from the cell surface and play a critical role in adhesion and invasion by pathogenic bacteria. The secretion of pili across the periplasm and outer membrane is mediated by a specialized secretin protein, PilQ, but the way in which this large channel is formed is unknown. Using NMR, we derived the structures of the periplasmic domains from N. meningitidis PilQ: the N-terminus is shown to consist of two β-domains, which are unique to the type IV pilus-dependent secretins. The structure of the second β-domain revealed an eight-stranded β-sandwich structure which is a novel variant of the HSP20-like fold. The central part of PilQ consists of two α/β fold domains: the structure of the first of these is similar to domains from other secretins, but with an additional α-helix which links it to the second α/β domain. We also determined the structure of the entire PilQ dodecamer by cryoelectron microscopy: it forms a cage-like structure, enclosing a cavity which is approximately 55 Å in internal diameter at its largest extent. Specific regions were identified in the density map which corresponded to the individual PilQ domains: this allowed us to dock them into the cryoelectron microscopy density map, and hence reconstruct the entire PilQ assembly which spans the periplasm. We also show that the C-terminal domain from the lipoprotein PilP, which is essential for pilus assembly, binds specifically to the first α/β domain in PilQ and use NMR chemical shift mapping to generate a model for the PilP:PilQ complex. We conclude that passage of the pilus fiber requires disassembly of both the membrane-spanning and the β-domain regions in PilQ, and that PilP plays an important role in stabilising the PilQ assembly during secretion, through its anchorage in the inner membrane.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. Conceived and designed the experiments: JPD LYL RCF TT. Performed the experiments: J-LB MMP TA LB RO RCF RFC SAF. Analyzed the data: MMP LYL J-LB RCF RFC JPD. Contributed reagents/materials/analysis tools: SAF TT. Wrote the paper: JPD MMP LYL J-LB RCF RFC TT.
ISSN:	1553-7374 1553-7366 1553-7374
DOI:	10.1371/journal.ppat.1002923