Chapter 14 : Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria

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Bacteria assemble a variety of adhesive proteins (adhesins) on their surface to mediate binding to receptors and colonization of surfaces. For pathogenic bacteria, adhesins are critical for early stages of infection, allowing the bacteria to initiate contact with host cells, colonize different tissues, and establish a foothold within the host. Adhesins recognize specific receptors expressed by specific subsets of host cells. Therefore, the repertoire of adhesins expressed by a pathogen play a major role in dictating the tropism of the pathogen toward specific host tissues and organs. Moreover, binding of bacterial adhesins to host cell receptors influences subsequent events by triggering signaling pathways in both the host and bacterial cells. These signaling pathways may determine whether the bacteria remain extracellular or become internalized, and influence the intracellular trafficking of invaded bacteria and their ability to survive and replicate ( ). The adhesins expressed by a pathogen are also critical for bacterial-bacterial interactions and the formation of bacterial communities, including biofilms. The ability to adhere to host tissues is particularly important for bacteria that colonize sites that include the urinary tract, where the flow of urine functions to maintain sterility by washing away non-adherent pathogens.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Image of Figure 1
Figure 1

Representative CU gene clusters and pili. Gene clusters coding for P (), type 1 () and Dr/Afa pili are depicted, with the functions of the genes indicated. Electron micrographs are shown for (A) an bacterium expressing type 1 pili, (B) a P pilus fiber, and (C) a type 1 pilus fiber. Scale bars equal 700 nm (A), 100 nm (B), and 20 nm (C). The images in panels A-C are reprinted from references , and , respectively, with permission of the publishers.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Image of Figure 2
Figure 2

Model for pilus biogenesis by the CU pathway. Pilus subunits enter the periplasm as unfolded polypeptides via the Sec system. Subunits fold upon forming binary complexes with the periplasmic chaperone (yellow). The crystal structure in the lower right depicts the chaperone-subunit donor strand exchange reaction (PapD-PapA; PDB ID: 2UY6), with the chaperone donor strand indicated in red. Pilus assembly takes place at the outer membrane usher, which catalyzes the exchange of chaperone-subunit for subunit-subunit interactions. Models for assembled P, type 1 and Afa/Dr pilus fibers are shown. The crystal structure in the upper left depicts the subunit-subunit donor strand exchange reaction that occurs in the pilus fiber (PapA-PapA; PDB ID: 2UY6), with the Nte donor strand indicated. Crystal structures of the PapG (P pili; PDB ID: 1J8R) and FimH (type 1 pili; PDB ID: 1KLF) adhesin domains with bound globoside and mannose, respectively. The sugars are depicted as dark gray spheres.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Image of Figure 3
Figure 3

Crystal structure of the FimD-FimC-FimH type 1 pilus assembly intermediate (PDB ID: 3RFZ). The Usher NTD, plug, β-barrel channel, and CTD domains are indicated. The FimH adhesin domain (FimH) is inserted inside the usher channel, and the FimH pilin domain (FimH) and bound FimC chaperone are located at the usher CTDs.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Image of Figure 4
Figure 4

Model for curli biogenesis by the extracellular nucleation/precipitation pathway. The gene cluster coding for curli biogenesis is shown at the bottom. The curli subunit proteins enter the periplasm via the Sec system and are secreted to the bacterial surface via the CsgG outer membrane channel. CsgE may act as a chaperone for the curli subunits in the periplasm, whereas CsgF assists assembly of CsgB on the cell surface. Polymerization of CsgA occurs on the cell surface and is nucleated by interaction with CsgB. Electron micrograph of expressing curli. Scale bar equals 1 µm; reprinted from reference ( ) with permission of the publisher. Structure of a CsgA subunit, with the R1-R5 repeats indicated.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Figure 5

Model for autotransporter secretion and assembly on the bacterial surface. The domain organization of an autotransporter protein is shown at the bottom. Autotransporter polypeptides have an N-terminal signal sequence for translocation to the periplasm via the Sec system. The protein is maintained in an extended, largely unfolded state during transit across the periplasm, assisted by periplasmic folding factors (SurA, Skp, DegP and FkpA). The C-terminal translocator domain inserts into the outer membrane as a β-barrel channel, with the assistance of the Bam complex. The Bam complex may also assist in secretion of the passenger domain to the cell surface. In the hairpin model of secretion, the C-terminal region of the passenger domain forms a hairpin structure in the translocator channel, exposing part of the passenger to the cell surface. Folding initiates at the autochaperone region, which then nucleates folding and secretion of the rest of the passenger domain. Following secretion, the linker region adopts an α-helical structure to plug the translocator domain channel. The passenger domain may remain linked to the translocator domain or may be proteolytically cleaved.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Figure 6

Crystal structures of representative autotransporter proteins. Translocator domains from the monomeric NalP and trimeric Hia autotransporters are shown (PDB IDs: 1UYN and 2GR7, respectively), with the β-barrel channels in blue and the α-helical linker regions in red. Passenger domains from the monomeric Pertactin and trimeric EibD autotransporters are shown (PDB IDs: 1DAB and 2XQH, respectively), with the approximate location of the Pertactin autochaperone region indicated in purple. The complete structure of the EstA autotransporter is shown (PDB ID: 3KVN), with the translocator domain in blue, the α-helical linker in red, and the globular passenger domain in gray.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Figure 7

Model for MSCRAMM secretion and incorporation into the cell wall. The domain organization of a typical MSCRAMM is shown at the bottom. MSCRAMMs have an N-terminal Sec signal sequence for translocation across the cytoplasmic membrane. The protein remains anchored in the cytoplasmic membrane by the CWSS. The positively charged C terminus remains in the cytoplasm, orienting the LPXTG motif to the extracellular side of the membrane. The SrtA sortase cleaves between the Thr and Gly of the MSCRAMM LPXTG motif, forming a covalent thioacyl intermediate. The MSCRAMM is then transferred to a lipid II peptidoglycan precursor and finally integrated into the cell wall at an amino acid cross-bridge. Crystal structures of the Ace and UafA MSCRAMMs (PDB IDs: 2Z1P and 3IRP, respectively). The upper structure shows the N and N subdomains of Ace in blue and green, respectively; the yellow circle represents bound collagen. Both domains have DEv-Ig folds. The C terminus of the N subdomain inserts into the N subdomain, forming a latch. The lower structure depicts the N, N, and B subdomains of UafA. The N and N subdomains adopt DEv-Ig folds and the B subdomain adopts a variant of the IgG-rev fold. The loop connecting the N and B domains (cyan) is thought to insert into the N subdomain upon ligand binding to form a latch.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Image of Figure 8
Figure 8

Crystal structures of representative tip and major pilins. The RrgA tip pilin of (PDB ID: 2WW8) is shown on the left, with the fold adopted by each of the four subdomains indicated. The VWA domain is depicted in green, with the residues forming the MIDAS motif and bound magnesium ion shown in purple. The residues involved in intramolecular isopeptide bond formation are shown in red. The Spy0128 major pilin of (PDB ID: 3B2M) is depicted on the right in purple and the two subdomains are labeled as for RrgA. The lysine side chain of Syp0128 thought to be involved in intermolecular isopeptide bond formation is shown in cyan.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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Figure 9

Model for Gram-positive pilus polymerization and incorporation into the cell wall. The domain organization of typical major and minor pilins is shown at the bottom, along with the gene cluster coding for Ebp pili of . The steps of secretion across the cytoplasmic membrane and covalent linkage to a sortase are the same as for MSCRAMMs, except the pilins are processed by the SrtC pilus-specific sortase. Pilus subunits are polymerized by formation of intermolecular isopeptide bonds between the Lys of a pilin motif of one subunit and the Thr of the LPXTG motif of a preceding subunit in the fiber. Linkage to the cell wall occurs when a growing pilus fiber is transferred to a base pilin bound to the SrtA housekeeping sortase. Integration of the pilus into the cell wall follows the mechanism as described for MSCRAMMs.

Citation: Chahales P, Thanassi D. 2017. Structure, Function, and Assembly of Adhesive Organelles by Uropathogenic Bacteria, p 277-329. In Mulvey M, Klumpp D, Stapleton A (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.UTI-0018-2013
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