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Chapter 24 : Type V Secretion in Gram-Negative Bacteria

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Abstract:

Type V, or “autotransporter,” secretion is an umbrella term that is often used to refer to a group of distinct but conceptually related protein export pathways that are widely distributed in Gram-negative bacteria. Autotransporters are generally single polypeptides that contain a signal peptide that promotes translocation across the inner membrane (IM) via the Sec pathway, an extracellular (“passenger”) domain, and a domain that anchors the protein to the outer membrane (OM). Passenger domains have a wide variety of functions, but they often promote virulence ( ). In the archetypical, or “classical” (type Va), autotransporter pathway, which was discovered in 1987, the passenger domain is located at the N terminus of the protein adjacent to the signal peptide ( ). Although passenger domains range in size from ∼20 to 300 kDa and are highly diverse in sequence ( ), X-ray crystallographic and studies predict that they usually fold into a repetitive structure known as a β helix ( ) ( Fig. 1 ). The membrane anchor domains are ∼30 kDa and are also highly diverse in sequence but contain short conserved sequence motifs ( ). Like most membrane-spanning segments associated with OM proteins (OMPs), these domains fold into a closed, amphipathic β sheet or “β barrel” structure. The C-terminal domains that have been crystallized to date all form nearly superimposable 12-stranded β barrels ( ). The two domains are connected by a short α-helical “linker” that is embedded inside the β barrel domain ( ). Many passenger domains are released from the cell surface by a proteolytic cleavage following their secretion ( ).

Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, p 307-318. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0031-2018
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Figures

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Figure 1

Proteins in type V (and type V-like) secretion pathways consist of a 12-stranded (red), 16-stranded (green), or predicted 8-stranded (pink) β barrel domain and an extracellular (“passenger”) domain that typically folds into a β-helical (blue), mixed coiled-coil/β roll/β prism (purple) or globular (brown) structure. The 16-stranded β barrel domains are members of the Omp85 superfamily and contain periplasmic POTRA domains. In most cases the β barrel and passenger domains are covalently linked, but in the type Vb pathway the β barrel domain and the extracellular component (“exoprotein”) are separate polypeptides. In the type Vc pathway both domains are formed through the assembly of three identical subunits. The passenger domain is located at the N terminus of the protein in the type Va, Vb, Vc, and Vd pathways, but it is found at the C terminus in the type Ve pathway. In the type V-like pathway the extracellular domain is located in a loop that connects the first two β strands of the β barrel domain. Crystal structures of representative polypeptides from each pathway are shown. α-helical segments are colored red and β strands are colored yellow. The structures include the pertactin (Prn) passenger domain ( ) (PDB code 1DAB), a fragment of the HMW1 exoprotein ( ) (PDB code 2ODL), a fragment of the EibD passenger domain ( ) (PDB code 2XQH), the phospholipase D (PlpD) passenger domain ( ) (PDB code 5FYA), the invasin (Inv) passenger domain ( ) (1CWV), the SabA extracellular domain ( ) (PDB code 4O5J), and the NalP, FhaC, Hia, and intimin (Int) β barrel domains (PDB codes 1UYO, 4QKY, 2GR7, and 4E1S) ( ). The helix inside the FhaC β barrel was generated from a neighboring asymmetric unit in the crystal lattice. No structures of β barrel domains of type Vd or type V-like proteins have been reported. Modified from ( ), with permission.

Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, p 307-318. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0031-2018
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Image of Figure 2
Figure 2

Available evidence suggests that the β barrel domain (red) begins to fold in the periplasm (step I) and incorporates the C terminus of the passenger domain (blue) in a hairpin conformation. At this stage the β barrel domain interacts with the molecular chaperone Skp. The partially folded β barrel domain is then targeted to the OM, where it binds to BamA, BamB, and BamD in a stereospecific fashion (step II). The surface exposure of the passenger domain and the initiation of translocation require an additional assembly step in which the β barrel domain moves into the membrane (step III). Both autotransporter and BamA β barrels are in an open conformation at this stage. Translocation involves the progressive movement of passenger domain segments from the chaperone SurA to the POTRA domains of BamA to the transport channel and is driven at least in part by vectorial folding (step IV). Following the completion of translocation the hairpin is resolved (step V), and an unusual lipid-facing basic or large polar residue found in at least a subset of autotransporters facilitates the completion of β barrel domain assembly (step VI). The β barrel domain is then released from the Bam complex, and, in some cases, the two domains are separated by an intrabarrel cleavage or an extrabarrel cleavage mediated by a -acting protease (step VII). In the Bam complex contains five subunits, but BamC and BamE have been omitted for clarity. Modified from ( ), with permission.

Citation: Bernstein H. 2019. Type V Secretion in Gram-Negative Bacteria, p 307-318. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/ecosalplus.ESP-0031-2018
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