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 2012-09, Vol.8 (9), p.e1002923-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: Article
Language:English
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)
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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.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1002923