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Review
. 2008 Sep 3;27(17):2271-80.
doi: 10.1038/emboj.2008.155.

Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria

Remi Fronzes  1 , Han Remaut, Gabriel Waksman
Affiliations
Review

Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria

Remi Fronzes et al. EMBO J. .

Abstract

Bacteria commonly expose non-flagellar proteinaceous appendages on their outer surfaces. These extracellular structures, called pill or fimbriae, are employed in attachment and invasion, biofilm formation, cell motility or protein and DNA transport across membranes. Over the past 15 years, the power of molecular and structural techniques has revolutionalized our understanding of the biogenesis, structure, function and mode of action of these bacterial organelles. Here, we review the five known classes of Gram-negative non-flagellar appendages from a biosynthetic and structural point of view.

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Figures

Figure 1
Figure 1
Pili and their assembly machineries in Gram-negative bacteria. Schematic view of the different pili found at the surface of Gram-negative bacteria. Chaperone–usher (CU) pili and curli are fibres attached on the cell surface. For the CU pili, both the P and type 1 pilus subunits and assembly proteins are shown. * indicates (1) that there are 5–10 PapE subunits in the tip fibrillum of the P pilus, whereas the equivalent subunit in the type 1 pilus system, FimF, is present in only one copy; (2) that the PapK adaptor between the PapE and PapA polymers does not have an equivalent in type 1 pili. CU pili and curli are assembled by simple systems located at the outer membrane. Type IV pili, type III secretion and type IV secretion pili are assembled by large multisubunit complexes crossing the whole bacterial cell envelope.
Figure 2
Figure 2
Pilins and pili structures. Chaperone–usher pathway: (top) crystal structure of PapD–PapA chaperone–subunit and PapA–PapA subunit–subunit complexes (Verger et al, 2007). (Bottom) Rod: cryo-EM density map (Mu and Bullitt, 2006) and model of the PapA rod (Sauer et al, 1999). (Bottom) Fibrillae: negative stain EM map (left) and model (right) of the SafA fibre (Salih et al, 2008). Curli: hypothetical CsgA and CsgB structure model (Barnhart and Chapman, 2006). Type IV pili: (top) structure of the N. gonorrhoeae GC pilin (type IVa pilin) (Craig et al, 2006) and V. cholerae TcpA pilin (type IVb pilin) (Craig et al, 2003). (Bottom) Cryo-EM density map of the GC pilus at 12.5 Å (left) and structural model of the pilin assembly within the pilus (right) (Craig et al, 2006). Type III secretion pili: (top) Shigella flexneri needle subunit MxiH crystal structure (Deane et al, 2006). (Bottom) cryo-EM density map of the S. flexneri needle and structural model of the pilin within the pilus (Deane et al, 2006). Type IV secretion pili: crystal structure of pKM101 Trac (VirB5 homologue) (Yeo et al, 2003).
Figure 3
Figure 3
Model of type 1 pilus assembly at the OM usher. The tip fibrillum of type 1 pili is composed of three single-copy subunits: FimH, the adhesin, and the FimG and FimF subunits. FimA is the major subunit of the type 1 pilus and is assembled immediately after FimF. In the type 1 pilus system, the chaperone is encoded by the fimC gene, whereas the usher is encoded by the fimD gene. Expression of the fimC, fimD, fimF, fimG and fimH genes results in the assembly of a FimD2:C:F:G:H complex where FimH is in donor-strand exchange with FimG, itself in donor-strand exchange with FimF. FimF is also in donor-strand complementation with FimC. In that complex, two protomers of FimD are present (Remaut et al, 2008). (A) The donor-strand complementation and donor-strand exchange mechanisms. (Top left) The subunit in red is shown in donor-strand complementation with the chaperone G1 strand in yellow. For clarity, only the F1 and G1 strands of the chaperone are shown. The A and F strands of the subunit are labelled. (Top right) The same subunit in red is shown in donor-strand exchange with the incoming subunit Nte (in cyan). For clarity, only the Nte peptide of that subunit is shown. (Bottom) Schematic representation of the concerted zip-in-zip-out donor-strand exchange mechanism. The diagrams show the F1-G1 β-hairpin (black) in the chaperone (yellow) and the A and F strands in the subunit (in red). The attacking Nte peptide is in cyan. (B) The type 1 FimD2:C:F:G:H complex in the process of recruiting a FimC:FimA complex. The model shows the FimD2:C:F:G:H complex as derived by cryo-EM (Remaut et al, 2008) coloured blue, dark blue, yellow, red orange and green for FimD usher pore 1, 2, the FimC chaperone, FimF, FimG and the FimH adhesin, respectively. In addition, the model shows the tentative position (shaded in light grey) of an incoming FimC:A complex bound to usher 2′s N-terminal domain (FimDN2:C:A, coloured dark blue, yellow, cyan, respectively, and labelled N2, FimC and FimA, respectively). N1 indicates the N-terminal domain of usher 1. The dashed rectangle labelled ‘A' refers to the region, the zoomed-in representation of which is shown in (A). (C) Schematic diagram of pilus assembly. The diagram shows the usher twinned pores (in blue and dark blue for usher 1 and 2, respectively), the ushers' N-terminal domains (N1 and N2 for usher 1 and 2 in blue and dark blue, respectively), the FimH adhesin (H; in green), FimG (G; in orange), FimC:F (C1:F; in yellow and red) and an incoming FimC:A complex (C2:A; in yellow and cyan). The plug domain is in magenta. As usher 2 is not used for secretion, the plug (P) remains in place obstructing the usher 2 pore. In the activated usher 1, two alternative positions are proposed (P′ and P′′): the plug could either move sideways (P′) or be ejected from the pore (P′). Note that the mechanism for pore activation or gating is unknown but is likely to be triggered by the binding of the chaperone–adhesin complex (Nishiyama et al, 2008; Remaut et al, 2008). For clarity, the C-terminal domains of usher 1 and 2 are not shown. At left, the FimD2:C:F:G:H complex (as represented in B) recruits an incoming FimC:A complex through binding to the N-terminal domain of usher 2 (N2; step 1). The complex is brought within donor-strand exchange of FimF, resulting in the release of the FimF-bound chaperone (C1) and the dissociation of the N-terminal domain of usher 1 (N1) (middle panel; steps 2 and 3). N1 is now free to recruit another FimC:A complex (labelled C:A′; right panel, step 4), and bring the complex within proximity of the N2-bound FimC:A complex (step 5). Donor-strand exchange then releases N2 for recruitment of the next chaperone–subunit complex (step 6). Iteration of alternating binding to released usher N-terminal domains, followed by donor-strand exchange with the penultimate chaperone–subunit complex leads to stepwise growth of the pilus fibre (steps 1 through 6).
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References

    1. Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, Koomey M (2002) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46: 749–760 - PubMed
    1. Akeda Y, Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911–915 - PubMed
    1. Anderson TF (1949) In The Nature of the Bacterial Surface, Miles AA, Pirie NW (eds), p 76 Oxford: Oxford University Press
    1. Balasingham SV, Collins RF, Assalkhou R, Homberset H, Frye SA, Derrick JP, Tonjum T (2007) Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J Bacteriol 189: 5716–5727 - PMC - PubMed
    1. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60: 131–147 - PMC - PubMed

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