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Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway

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  • Authors: Zachary M. Nash1, Peggy A. Cotter2
  • Editors: Maria Sandkvist3, Eric Cascales4, Peter J. Christie5
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    Affiliations: 1: Department of Microbiology and Immunology, University of North Carolina—Chapel Hill, Chapel Hill, NC 27599; 2: Department of Microbiology and Immunology, University of North Carolina—Chapel Hill, Chapel Hill, NC 27599; 3: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 4: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 5: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0024-2018
  • Received 11 December 2018 Accepted 08 February 2019 Published 29 March 2019
  • Peggy A. Cotter, [email protected]
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  • Abstract:

    Bacteria use a variety of mechanisms to translocate proteins from the cytoplasm, where they are synthesized, to the cell surface or extracellular environment or directly into other cells, where they perform their ultimate functions. Type V secretion systems (T5SS) use β-barrel transporter domains to export passenger domains across the outer membranes of Gram-negative bacteria. Distinct among T5SS are type Vb or two-partner secretion (TPS) systems in which the transporter and passenger are separate proteins, necessitating a mechanism for passenger-translocator recognition in the periplasm and providing the potential for reuse of the translocator. This review describes current knowledge of the TPS translocation mechanism, using filamentous hemagglutinin (FHA) and its transporter FhaC as a model. We present the hypothesis that the TPS pathway may be a general mechanism for contact-dependent delivery of toxins to target cells.

  • Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway. Microbiol Spectrum 7(2):PSIB-0024-2018. doi:10.1128/microbiolspec.PSIB-0024-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.PSIB-0024-2018
2019-03-29
2019-08-22

Abstract:

Bacteria use a variety of mechanisms to translocate proteins from the cytoplasm, where they are synthesized, to the cell surface or extracellular environment or directly into other cells, where they perform their ultimate functions. Type V secretion systems (T5SS) use β-barrel transporter domains to export passenger domains across the outer membranes of Gram-negative bacteria. Distinct among T5SS are type Vb or two-partner secretion (TPS) systems in which the transporter and passenger are separate proteins, necessitating a mechanism for passenger-translocator recognition in the periplasm and providing the potential for reuse of the translocator. This review describes current knowledge of the TPS translocation mechanism, using filamentous hemagglutinin (FHA) and its transporter FhaC as a model. We present the hypothesis that the TPS pathway may be a general mechanism for contact-dependent delivery of toxins to target cells.

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Figures

Image of FIGURE 1
FIGURE 1

Structures of FhaC and the TPS domain of FhaB. Helix 1 (H1; orange) and loop 6 (L6; fuchsia) are located within the pore of the 16-stranded β barrel (blue) of FhaC when the transporter is in the “closed” state. The POTRA domains (POTRA1 and POTRA2; red) remain periplasmic for selective recognition of the FhaB TPS domain. The TPS domain of FhaB adopts a triangular β-helical structure, shown from the side of the helix (left) and top down in a C-terminal to N-terminal direction (right). Termini are indicated by outlined letters.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0024-2018
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Image of FIGURE 2
FIGURE 2

Initial steps in secretion of FhaB. FhaC alternates between a closed state, in which H1 (orange) and L6 (fuchsia) plug the channel, and an open state, in which H1 and L6 localize to the periplasm and the extracellular space, respectively. The POTRA domains of FhaC (red) bind the unfolded FhaB TPS domain (green line), stabilizing FhaC in the open state. The N terminus of FhaB then binds the interior of the FhaC barrel at β-strands B5 to B8 (blue asterisk) and forms into a β-helix as the protein is translocated, preventing backsliding through the channel.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0024-2018
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Image of FIGURE 3
FIGURE 3

Two models for FhaB secretion: distal N-terminus versus hairpin. In the model proposed by Coutte et al. ( 38 ) , the N terminus of FhaB is pushed away from the membrane as more of the polypeptide translocates through FhaC. The protease SphB1 cleaves between the mature C-terminal domain (MCD) and the periplasmic prodomain, causing release of FHA. In the alternative “hairpin” model proposed by Mazar and Cotter ( 34 ) , the N terminus of FhaB remains bound to FhaC during secretion, and the MCD is located at the distal end of the β-helix. A portion of the MCD spans the helix length, as it is tethered to the periplasmic prodomain. The prodomain N terminus (PNT) prevents translocation of the prodomain through FhaC.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0024-2018
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Image of FIGURE 4
FIGURE 4

Model for stepwise processing and release of FhaB. Upon receipt of an unknown maturation signal (yellow bolt), an as-yet-unidentified protease (P3) removes the extreme C terminus (ECT) and exposes a substrate for the protease CtpA. CtpA processively degrades the prodomain through a portion of the PNT, forming FHA′ and shifting the polypeptide to expose the cleavage site of SphB1. FHA is formed from SphB1-dependent cleavage of FHA′, and it is retained at the membrane until the remaining portion of the prodomain exits FhaC (gray barrel).

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0024-2018
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