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Chapter 31 : A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective

Authors: Natalie Zeytuni, Natalie C.J. Strynadka
Content Type: Monograph
Publication Year: 2019

Category: Bacterial Pathogenesis

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Abstract:

Bacteria utilize sophisticated nanomachines to transport proteins, small molecules, and DNA across membranes to the extracellular environment. These transport machineries, also known as secretion systems, are involved in various cellular functions, such as adhesion to surfaces or host cells, cell-cell communication, motility (flagella), virulence effector protein secretion, and, notably, bacterial pathogenesis ( ). Several of the identified protein secretion systems comprise large complexes that localize and assemble in and around the bacterial membrane(s), forming specialized channels through which the selected substrate(s) is actively delivered ( ). Although exhibiting significant diversity in structure, substrate, and function, the dedicated type II, III, IV, and IV-pilus secretion systems (T2SS, T3SS, T4SS, and T4PS, respectively) in didermic Gram-negative bacteria each transport a specific subset of proteins to the extracellular milieu via passage through large stacked ring-shaped channels that span the inner membrane (IM) and outer membrane (OM).

Citation: Zeytuni N, Strynadka N. 2019. A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective, p 389-399. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0013-2018
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A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective
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Citation: Zeytuni N, Strynadka N. 2019. A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective, p 389-399. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0013-2018
/content/10.1128/9781683670285.chap31.fig31-1
Figure 1
Schematic representation of the sporulation process and the active sporulation channel architecture model. (Top) Morphological changes mediated by cell-specific sigma factors that regulate gene expression in . (Bottom) Sporulation channel assembly and function during the engulfment stage involve the expression of nine core component proteins forming a channel that crosses the mother cell membrane, the transenvelope space, and the forespore membrane. (Left) Monomeric topology and known structures of the essential core proteins. (Right) Schematic illustration of the suggested model of the assembled SpoIIIA-IIQ channel. Based on the similarities of the individual components to proteins from other bacterial secretion systems, it is predicted that the core components oligomerize into ring-like structures that are stacked to form this sporulation-specialized secretion system. In this model, the stacked rings of SpoIIIAF, SpoIIIAG, and SpoIIIAH-SpoIIQ form the main conduit in the transenvelope space connecting the mother cell and the forespore. SpoIIIAC and SpoIIIAD form a simplified version of an export apparatus through the mother cell membrane. SpoIIIAE utilizes the proton motif force for substrate transportation and also to mediate the interaction with the SpoIIIAA ATPase and its possible docking platform formed by oligmerized (?) SpoIIIAB. Any additional pore-forming protein(s) required at the forespore membrane has yet to be identified.
10.1128/9781683670285/fig31-1_thmb.gif
10.1128/9781683670285/fig31-1.gif
Image of Figure 1
Figure 1

Schematic representation of the sporulation process and the active sporulation channel architecture model. (Top) Morphological changes mediated by cell-specific sigma factors that regulate gene expression in . (Bottom) Sporulation channel assembly and function during the engulfment stage involve the expression of nine core component proteins forming a channel that crosses the mother cell membrane, the transenvelope space, and the forespore membrane. (Left) Monomeric topology and known structures of the essential core proteins. (Right) Schematic illustration of the suggested model of the assembled SpoIIIA-IIQ channel. Based on the similarities of the individual components to proteins from other bacterial secretion systems, it is predicted that the core components oligomerize into ring-like structures that are stacked to form this sporulation-specialized secretion system. In this model, the stacked rings of SpoIIIAF, SpoIIIAG, and SpoIIIAH-SpoIIQ form the main conduit in the transenvelope space connecting the mother cell and the forespore. SpoIIIAC and SpoIIIAD form a simplified version of an export apparatus through the mother cell membrane. SpoIIIAE utilizes the proton motif force for substrate transportation and also to mediate the interaction with the SpoIIIAA ATPase and its possible docking platform formed by oligmerized (?) SpoIIIAB. Any additional pore-forming protein(s) required at the forespore membrane has yet to be identified.

Citation: Zeytuni N, Strynadka N. 2019. A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective, p 389-399. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0013-2018
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Figure 2
Structures of the core components of the sporulation channel share similar structural motifs with homologs from other bacterial secretion systems. (Top) The SpoIIIAB soluble domain adopts a six-helix bundle fold with both N and C termini in close proximity and facing the mother cell membrane. The molecule is shown in two views, related by a 90° rotation. (Bottom) SpoIIIAB shares a fold similar to that of homologous proteins from the T2SS and T4PS. Shown is a structural overlay of SpoIIIAB with EpsF, TcpE (both from ), and PilC () proteins in blue, wheat, green, and pink, respectively (PDB codes 6BS9, 3C1Q, 2WHN, and 4HHX, respectively). Two regions of structural variation are seen in the helix 6 angle and the increasing dimensions of helices 4 and 5 and the loop connecting them. SpoIIIAF, SpoIIIAG, and the SpoIIIAH-SpoIIQ heterodimer contain an RBM fold similar to that of the T3SS basal body proteins, EscJ () and PrgK ( Tryphimurium) (PDB codes 6DCS, 5WC3, 3UZ0, 1YJ7, and 3J6D, respectively). All five structures are displayed in cartoon representation and rainbow color scheme and for clarity are individually shown in identical orientations originating from structural superposition. SpoIIIAF is presented as an overlay of the two monomers seen in the crystal structure, with the region of alternate conformation associated with regulation marked with an asterisk. SpoIIIAG adopts the canonical RBM fold, with a large insertion of the β-triangle motif marked with an asterisk. An SpoIIIAH additional N-terminal helix is marked with an asterisk. Cryo-EM structure of the SpoIIIAG soluble domain 30-meric ring. A three-dimensional reconstruction and atomic model are shown in top side, cropped, and tilted views. The SpoIIIAG ring structure is colored according to distinctive ring elements: RBM in cyan, planar β-ring in green, and vertical β-ring in pink, with the single protomer in red. SpoIIIAH-SpoIIQ representative computational modeled ring, here in C15 symmetry with zoomed-in view of the predicted interaction region between the RBMs of SpoIIIAH. Ring model coordinates were obtained from Meisner et al. ( ).
10.1128/9781683670285/fig31-2_thmb.gif
10.1128/9781683670285/fig31-2.gif
Image of Figure 2
Figure 2

Structures of the core components of the sporulation channel share similar structural motifs with homologs from other bacterial secretion systems. (Top) The SpoIIIAB soluble domain adopts a six-helix bundle fold with both N and C termini in close proximity and facing the mother cell membrane. The molecule is shown in two views, related by a 90° rotation. (Bottom) SpoIIIAB shares a fold similar to that of homologous proteins from the T2SS and T4PS. Shown is a structural overlay of SpoIIIAB with EpsF, TcpE (both from ), and PilC () proteins in blue, wheat, green, and pink, respectively (PDB codes 6BS9, 3C1Q, 2WHN, and 4HHX, respectively). Two regions of structural variation are seen in the helix 6 angle and the increasing dimensions of helices 4 and 5 and the loop connecting them. SpoIIIAF, SpoIIIAG, and the SpoIIIAH-SpoIIQ heterodimer contain an RBM fold similar to that of the T3SS basal body proteins, EscJ () and PrgK ( Tryphimurium) (PDB codes 6DCS, 5WC3, 3UZ0, 1YJ7, and 3J6D, respectively). All five structures are displayed in cartoon representation and rainbow color scheme and for clarity are individually shown in identical orientations originating from structural superposition. SpoIIIAF is presented as an overlay of the two monomers seen in the crystal structure, with the region of alternate conformation associated with regulation marked with an asterisk. SpoIIIAG adopts the canonical RBM fold, with a large insertion of the β-triangle motif marked with an asterisk. An SpoIIIAH additional N-terminal helix is marked with an asterisk. Cryo-EM structure of the SpoIIIAG soluble domain 30-meric ring. A three-dimensional reconstruction and atomic model are shown in top side, cropped, and tilted views. The SpoIIIAG ring structure is colored according to distinctive ring elements: RBM in cyan, planar β-ring in green, and vertical β-ring in pink, with the single protomer in red. SpoIIIAH-SpoIIQ representative computational modeled ring, here in C15 symmetry with zoomed-in view of the predicted interaction region between the RBMs of SpoIIIAH. Ring model coordinates were obtained from Meisner et al. ( ).

Citation: Zeytuni N, Strynadka N. 2019. A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective, p 389-399. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0013-2018
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