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Chapter 12 : The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective

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Abstract:

Chaperone-usher (CU) pili are virulence factors displayed on a wide variety of Gram-negative bacterial pathogens ( ), mediating bacterial attachment and biofilm formation ( ). The two best-studied examples of CU pili are the type 1 and P pili of uropathogenic (UPEC), which is the most important causative agent of urinary tract infections ( ). We here summarize the steps of CU pilus biogenesis and highlight the most recent structural advances relating to type 1 pili that allow UPEC to thrive in the urinary tract.

Citation: Hospenthal M, Waksman G. 2019. The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective, p 137-148. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0010-2018
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Figure 1

Architecture and assembly of chaperone-usher pili. Type 1 (left) and P pili (right) are the two archetypal CU pili of UPEC. Pilins are transported through the inner membrane (IM) via the SecYEG machinery. Once in the periplasm, a dedicated chaperone (FimC for type 1 pili; PapD for P pili) helps to fold, stabilize, and transport individual pilins to the outer membrane (OM), where they are assembled into pili by the usher (FimD for type 1 pili; PapC for P pili). The largest section of CU pili is the rod, which is composed of thousands of copies of a single subunit (FimA for type 1 pili; PapA for P pili) arranged into a right-handed superhelical quaternary structure. On top of the rod, located at the pilus’ distal end, is a thin and flexible tip fibrillum. The most important tip fibrillum subunit is the adhesin (FimH for type 1 pili; PapG for P pili), which is responsible for the interaction of CU pili with host cell receptors. The remainder of the tip fibrillum is formed by FimG and FimF for type 1 pili and PapF, PapE, and PapK for P pili. Pilins are unstable on their own because they consist of C-terminally truncated incomplete Ig-like folds lacking the 7th β-strand. This creates a large hydrophobic groove on the subunit’s surface. After their transport into the periplasm, the chaperone inserts its G1 β-strand into the hydrophobic groove, thereby completing and stabilizing its fold. This is known as donor strand complementation (DSC) (PDB code 4DWH [ ]) (left side). The pilin’s P1 to P4 pockets are occupied by the chaperone’s P1 to P4 residues, while the P5 pocket remains empty. Once assembled into a pilus, the 10- to 20-residue-long N-terminal extension (Nte) of each subunit complements the preceding pilin’s groove, stabilizing the structure and linking the subunits in the pilin polymer. This is referred to as donor strand exchange (DSE) (PDB code 5OH0 [ ]) (right side). The Nte of FimA in the surface model on the right has been removed for clarity. A zip-in–zip-out mechanism is responsible for the transition from DSC to DSE, whereby the previously empty P5 pocket first becomes occupied by the incoming subunit’s Nte, displacing the chaperone’s complementing strand and subsequently allowing the Nte to fully occupy the pilin’s P1 to P5 pockets. In step 1, the chaperone-adhesin complex binds to the usher’s NTD (PDB codes 3BWU [ ], 1QUN [ ], and 3OHN and 3RFZ [ ]). In step 2, the plug relocates next to the periplasmically located NTD, while the chaperone-adhesin complex is transferred to the usher’s CTDs, which interact with the adhesin’s pilin domain. The adhesin’s lectin domain begins to translocate through the usher pore (PDB code 3RFZ). In step 3, the next chaperone-pilin complex is recruited to the NTD and the Nte of this pilin is oriented towards the pilin domain of the adhesin (PDB codes 3RFZ and 3BWU). In step 4, the chaperone’s donor strand is replaced by the Nte of the newly recruited pilin by the zip-in–zip-out mechanism. The displaced chaperone is recycled (PDB codes 3RFZ, 3BWU, and 4XOE [ ]). In step 5, the chaperone-pilin complex is transferred to the CTDs and the adhesin continues to move up and out through the usher pore (PDB codes 3RFZ and 4J3O [ ]). In step 6, the cycle is repeated and new pilins are incorporated into the growing pilus (PDB code 4J3O). The mechanism of translocation through the usher depicted is illustrated using both crystal and modeled structures of the CU pilus systems. Two novel structures shed light on the chaperone-subunit handover mechanism from the NTD to the CTDs. Shown are the structures of PapCDG (PDB code 6CD2 [ ]) in a preactivated state and of FimDCFGH (PDB code 6E14 [ ]) in an activated state , trapping conformations that show novel interactions between the NTD and CTD2, during chaperone-subunit handover. Dashed boxes and zoomed-in views highlight the NTD to CTD2 interactions.

Citation: Hospenthal M, Waksman G. 2019. The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective, p 137-148. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0010-2018
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Image of Figure 2
Figure 2

Structural rearrangements in FimH. Ribbon diagram of full-length FimH (yellow), which is complemented by a donor strand peptide from FimG (orange) (PDB code 4XOE [ ]). The lectin and pilin domains are labeled, and the dashed boxes highlight the ligand binding pocket (top) and the domain interface region (bottom) that are expanded in panels b and c. Superposition of apo (gray) (PDB code 4XOD [ ]) and ligand-bound (cyan) (PDB code 4XOE [ ]) FimH, focusing on the ligand binding pocket. The ligand is -heptyl α-d-mannoside (HM). An arrow indicates the structural rearrangement of the clamp loop. Superposition of ligand-bound FimH (cyan) (PDB code 4XOE) and a ligand-bound construct of the FimH lectin domain only (purple) (PDB code 4XOC [ ]), focusing on the lectin domain loops at the domain interface. The cyan structure is in a domain-associated (low-affinity) state, whereas the purple lectin domain-only structure represents the conformation of a domain-separated (high-affinity) state. Arrows indicate the rearrangements of the swing, linker, and insertion loops. The FimH pilin domain in all structures was stabilized by a FimG donor strand peptide.

Citation: Hospenthal M, Waksman G. 2019. The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective, p 137-148. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0010-2018
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Figure 3

The structure of the rod. Surface models showing the type 1 pilus rod structure (PDB code 5OH0 [ ]) in a side view and a top view, which are 90° rotated with respect to each other. The Nte of the uppermost FimA molecule is removed in the top view for illustrative purposes. Cartoon models showing three adjacent molecules or one “stack” of the type 1 pilus (blue) (PDB code 5OH0) and P pilus (green) (PDB code 5FLU [ ]) rods. The left and right parts of this panel show one stack as a side view and a top view, respectively, rotated by 90°. Pilin subunits are arbitrarily numbered starting with the pilin at the bottom, which would be most proximal to the OM and last to be assembled, to show the nature of the right-handed superhelical structure. The arrow in the side view shows the upward trajectory of the subunits in the structure. Surface representation of an individual FimA pilin subunit within the type 1 pilus rod (left, blue) (PDB code 5OH0) and a PapA pilin subunit within the P pilus rod (right, green) (PDB code 5FLU). The stick model shows the complementing donor strands, which originate from the Nte of the next subunit in assembly. The dashed box shows the staple region (residues 1 to 5) of the PapA Nte, a region not present in the type 1 pilus.

Citation: Hospenthal M, Waksman G. 2019. The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective, p 137-148. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0010-2018
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