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DNA Uptake by Type IV Filaments

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Review

DNA Uptake by Type IV Filaments

Kurt H Piepenbrink. Front Mol Biosci.

Abstract

Bacterial uptake of DNA through type IV filaments is an essential component of natural competence in numerous gram-positive and gram-negative species. Recent advances in the field have broadened our understanding of the structures used to take up extracellular DNA. Here, we review seminal experiments in the literature describing DNA binding by type IV pili, competence pili and the flp pili of Micrococcus luteus; collectively referred to here as type IV filaments. We compare the current state of the field on mechanisms of DNA uptake for these three appendage systems and describe the current mechanistic understanding of both DNA-binding and DNA-uptake by these versatile molecular machines.

Keywords: DNA-binding; Flp pili; competence pili; horizontal gene transfer; natural competence; type IV pili.

Figures

Figure 1
Figure 1
Schematics of T4F systems. Major pilin proteins are depicted in blue, minor pilin proteins in green, orange and yellow, putative extension ATPase proteins in green, retraction ATPases in red, PilC homologs in yellow and ComEC in orange. (A) type IV pili from a Gram-negative species, (B) competence pili from a Gram-positive species and (C) Flp pili from M. luteus.
Figure 2
Figure 2
ComP, the pilin DNA receptor from Neisseria. (A) (left) ribbon diagram of ComP in gold, (right) columbic electrostatic surface calculation of ComP, (B) schematics of Neisseria type IV pili showing the major pilin, PilE, as well as a putative tip complex containing PilK, PilJ, PilI, PilH, PilX, PilC, and either ComP or PilV. (C) Superimposition of ComP (gold) and PilV (blue).
Figure 3
Figure 3
Neisseria gonnorheae type IV pili. (A) Ribbon diagram of PilE monomer. (B) Structure of a N. gonnorheae type IV pilus (PDBID: 5VXX). (C) Salt bridges between the side-chain of glutamate 5 and the amino terminus (F1) of the i + 1 pilin, 3DEM electron density is shown as a blue mesh.
Figure 4
Figure 4
Streptococcus pneumoniae competence pili. (A) Ribbon diagram of a modeled full-length ComGC monomer (model 1). (B) Model of a S. pneumoniae pilus, centroids from the α2 and α3 helices are shown as spheres. (C) Superimposition of 20 models from the ComGC NMR structure (PDBID: 5NCA).
Figure 5
Figure 5
Minimal pilus filaments. (A) Model of an Flp pilus from M. luteus. (B) Model of a full-length monomer of the Flp pilin. (C) Model of the N-terminal portion of PilE after S-pilin cleavage. The N-pilin in depicted in gold, the S-pilin is shown in transparent gray. (D) Model of a filament composed of N-pilins.
Figure 6
Figure 6
T4F ATPase motor proteins. (A) Structure of hexameric PilT from Aquifex aeolicus with each monomer in a different color (PDB ID: 2GSZ) (B) Monomer of PilT from panel A showing the two domains. (C) Aligned PilB (P. stutzeri), PilT (P. stutzeri), ComGA (S. pneumoniae), and TadA (M. luteus) sequences. (D) Phylogenetic tree of putative motor proteins showing PilB (from T. thermophilus, H. influenza, M. catarrhalis, N. meningitidis, P. stutzeri, and A. nosocomialis), ComGA (from B. subtilis, S. aureus, and S. pneumoniae), PilT/U (from A. nosocomialis, P. stutzeri, T. thermophiles, and M. catarrhalis), and TadA (M. luteus) branches.
Figure 7
Figure 7
Diagrams of DNA-binding (top) and DNA-uptake (bottom) by T4F. DNA-binding is depicted by the major pilin (left), a tip complex (center) and minor pilins along the pilus length (right). DNA uptake is depicted by retraction through the secretin (or equivalent pore) (left), by diffusion through another channel (center) and by diffusion through an empty secretin-like channel (right).

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References

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