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Chapter 25 : Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway

Authors: Zachary M. Nash, Peggy A. Cotter
Content Type: Monograph
Publication Year: 2019

Category: Bacterial Pathogenesis

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Abstract:

Bacteria use surface molecules to interact with inanimate objects during biofilm development, other bacteria during sociomicrobiological community activities, and host organisms during mutualistic, commensal, and parasitic symbioses. Among the mechanisms for delivering proteins to the surface of Gram-negative bacteria are type V secretion systems (T5SS) ( ). T5SS comprise a passenger domain and an associated β-barrel transporter domain that, once integrated into the outer membrane via the Bam assembly complex, is sufficient for export of the passenger from the periplasm to the cell surface. Based on domain architecture, T5SS are categorized into five classes, with type Vb or two-partner secretion (TPS) pathway systems being distinct because the passenger domain (referred to generically as a TpsA protein) is synthesized independently from the transporter domain (the TpsB protein). This arrangement requires a mechanism for passenger-transporter recognition in the periplasm and may allow reuse of the transporter for export of multiple copies of the same, or closely related, passenger proteins.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Bordetella Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway
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Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
/content/10.1128/9781683670285.chap25.fig25-1
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.
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10.1128/9781683670285/fig25-1.gif
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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.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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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.
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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.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Figure 3
Two models for FhaB secretion: distal N-terminus versus hairpin. In the model proposed by Coutte et al. ( ) , 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 ( ) , 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.
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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. ( ) , 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 ( ) , 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.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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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).
10.1128/9781683670285/fig25-4_thmb.gif
10.1128/9781683670285/fig25-4.gif
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).

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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