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EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways

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  • Author: Harris D. Bernstein1
  • Editors: James M. Slauch2, Harris Bernstein3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892; 2: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL; 3: National Institutes of Health, Bethesda, MD
  • Received 07 December 2009 Accepted 15 February 2010 Published 16 September 2010
  • Address correspondence to Harris D. Bernstein harris_bernstein@nih.gov
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  • Abstract:

    The autotransporter and two-partner secretion (TPS) pathways are used by and many other Gram-negative bacteria to delivervirulence factors into the extracellular milieu.Autotransporters arecomprised of an N-terminal extracellular ("passenger") domain and a C-terminal β barrel domain ("β domain") that anchors the protein to the outer membrane and facilitates passenger domain secretion. In the TPS pathway, a secreted polypeptide ("exoprotein") is coordinately expressed with an outer membrane protein that serves as a dedicated transporter. Bothpathways are often grouped together under the heading "type V secretion" because they have many features in common and are used for the secretion of structurally related polypeptides, but it is likely that theyhave distinct evolutionary origins. Although it was proposed many years ago that autotransporterpassenger domains are transported across the outer membrane through a channel formed by the covalently linked β domain, there is increasing evidence that additional factors are involved in the translocation reaction. Furthermore, details of the mechanism of protein secretion through the TPS pathway are only beginning to emerge. In this chapter I discussour current understanding ofboth early and late steps in the biogenesis of polypeptides secreted through type V pathways and current modelsofthe mechanism of secretion.

  • Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6

Key Concept Ranking

Outer Membrane Proteins
0.4353282
Viral Capsid Proteins
0.40876362
BAM Complex Proteins
0.39504206
0.4353282

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/content/journal/ecosalplus/10.1128/ecosalplus.4.3.6
2010-09-16
2017-12-13

Abstract:

The autotransporter and two-partner secretion (TPS) pathways are used by and many other Gram-negative bacteria to delivervirulence factors into the extracellular milieu.Autotransporters arecomprised of an N-terminal extracellular ("passenger") domain and a C-terminal β barrel domain ("β domain") that anchors the protein to the outer membrane and facilitates passenger domain secretion. In the TPS pathway, a secreted polypeptide ("exoprotein") is coordinately expressed with an outer membrane protein that serves as a dedicated transporter. Bothpathways are often grouped together under the heading "type V secretion" because they have many features in common and are used for the secretion of structurally related polypeptides, but it is likely that theyhave distinct evolutionary origins. Although it was proposed many years ago that autotransporterpassenger domains are transported across the outer membrane through a channel formed by the covalently linked β domain, there is increasing evidence that additional factors are involved in the translocation reaction. Furthermore, details of the mechanism of protein secretion through the TPS pathway are only beginning to emerge. In this chapter I discussour current understanding ofboth early and late steps in the biogenesis of polypeptides secreted through type V pathways and current modelsofthe mechanism of secretion.

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Figures

Image of Figure 1
Figure 1

Classical autotransporters (A) are single polypeptides consisting of a large N-terminal extracellular domain (passenger domain) and a ~30-kDa β-barrel domain (β domain) that resides in the OM. Trimeric autotransporters (B) are homooligomers consisting of three intertwined passenger domains and three ~80-kDa β domains that form a single β barrel. In two-partner secretion (C), a large secreted polypeptide (“TpsA” or “exoprotein”) and its ~60-kDa transporter (“TpsB”) are encoded as separate polypeptides within a single operon. The passenger domains of classical autotransporters and TpsA molecules (dark blue) are predominantly β helical, while the passenger domains of trimeric autotransporters (light blue) contain distinct β-solenoid structural elements. The β domains of classical and trimeric autotransporters (green) are structurally closely related. TpsB proteins, however, consist of a ~20-kDa N-terminal periplasmic domain (brown) and a very different β barrel (orange).

Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6
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Figure 2

Top, crystal structures of secreted polypeptides. The structures of the passenger domains of the classical autotransporters pertactin (Prn) and Hbp are shown ( 15 , 17 ). The structures of the collagen-binding domain of the trimeric autotransporter YadA (residues 26 to 241) and the TPS domain of the exoprotein FHA (residues 72 to 375) are also shown ( 25 , 30 ). β strands are yellow, and α helices are red, with the exception of YadA, where individual subunits are blue, orange, and yellow. Bottom, crystal structures of OM components. Structures of the β domains of the classical autotransporters NalP and EspP and the trimeric autotransporter Hia are shown ( 31 , 32 , 33 ). The structure of the TpsB protein FhaC is also shown ( 34 ). β strands are yellow, and α helices are red, with the exception of Hia, where individual subunits are blue, orange, and yellow. Adapted with permission from ref. 35 a.

Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6
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Image of Figure 3
Figure 3

Members of the BamA superfamily are found in the bacterial, mitochondrial, and chloroplast OMs. Some members of the family have been implicated in membrane protein integration reactions, whereas others promote protein translocation. All family members have between one and five N-terminal POTRA domains and an ~40-kDa membrane-embedded β-barrel domain. Two sequence motifs (designated motifs 3 and 4; see reference 57 ) are conserved throughout the BamA superfamily. TpsB proteins also contain an N-terminal α-helix that is connected to the rest of the protein by an unstructured linker (light blue).

Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6
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Figure 4

Top, models of the mechanism of autotransporter secretion. In the self-transport (or “hairpin”) model (A), the passenger domain is secreted by the covalently linked β domain. The C terminus of the passenger domain first forms a hairpin that is embedded inside the β-domain pore. Subsequently, segments of the passenger domain are threaded through the β-domain pore in a C- to N-terminal direction until the entire polypeptide reaches the extracellular milieu. In the facilitated transport model (B), the passenger domain is extruded across the OM in a C- to N-terminal direction by the Bam complex or another external transporter by an unknown mechanism. In this model, the primary role of the β domain is to target the passenger domain to the appropriate transport factor. In both of these models a segment of the passenger domain is incorporated into the β domain prior to its integration into the OM. Although only a classical autotransporter is depicted, it is likely that trimeric autotransporters utilize a similar secretion mechanism. Bottom, model of the mechanism of two-partner secretion (C). In this model, an interaction between the TPS domain of TpsA and the TpsB POTRA domains gates opens the pore of the TpsB β barrel by catalyzing a conformational change in loop 6 (L6). TpsA is then threaded through the pore in an N- to C-terminal fashion. After the C terminus of the protein is transported through the pore the N terminus dissociates from the POTRA domains and is secreted. The highly conserved VRGY motif in L6 is green. It should be noted that in all of these models the vectorial folding of the passenger domain or TpsA protein in the extracellular space drives translocation by preventing the secreted polypeptide from sliding back through the translocation channel. Adapted with permission from ref. 35 a.

Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6
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Figure 5

Top, mechanisms of passenger domain cleavage. (A) The passenger domain of IcsA (blue) is cleaved by a dedicated protease called IcsP (pink). (B) The passenger domains of the IgA protease (IgaP) and App are cleaved by NalP and are processed further in an autocatalytic reaction to release a small C-terminal α fragment. It is not known whether the latter reaction is intramolecular or intermolecular. (C) The passenger domain of Hap is cleaved in an intermolecular autoproteolytic reaction. (D) AIDA-I is cleaved near the C terminus of the passenger domain in an intramolecular reaction that involves acidic residues. (E) The passenger domains of the SPATEs and the pertactin (Prn) family of autotransporters are released in an intrabarrel autocatalytic reaction. Bottom, mechanisms of exoprotein processing. (F) The C-terminal ~1,200 residues of FHA are removed from the protein by the autotransporter SphB1. It is not known whether the C-terminal pro domain is cleaved prior to its translocation across the OM, but it appears to be rapidly degraded. (G) The N-terminal ~370 residues of HMW1 are also released in a proteolytic reaction. The identity of the protease is not known, but the pro domain is probably cleaved after its secretion. HMW1 is anchored to the OM by a C-terminal disulfide bond. Adapted with permission from ref. 35 a.

Citation: Bernstein H. 2010. Type V Secretion: the Autotransporter and Two-Partner Secretion Pathways, EcoSal Plus 2010; doi:10.1128/ecosalplus.4.3.6
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