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A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective

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  • Authors: Natalie Zeytuni1, Natalie C.J. Strynadka2
  • Editors: Maria Sandkvist3, Eric Cascales4, Peter J. Christie5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biochemistry and Molecular Biology and the Center for Blood Research, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4; 2: Department of Biochemistry and Molecular Biology and the Center for Blood Research, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4; 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 January 2019 vol. 7 no. 1 doi:10.1128/microbiolspec.PSIB-0013-2018
  • Received 04 September 2018 Accepted 06 December 2018 Published 25 January 2019
  • Natalie Zeytuni, [email protected]
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  • Abstract:

    Bacteria employ a number of dedicated secretion systems to export proteins to the extracellular environment. Several of these comprise large complexes that assemble in and around the bacterial membrane(s) to form specialized channels through which only selected proteins are actively delivered. Although typically associated with bacterial pathogenicity, a specialized variant of these secretion systems has been proposed to play a central part in bacterial sporulation, a primitive protective process that allows starving cells to form spores that survive in extreme environments. Following asymmetric division, the mother cell engulfs the forespore, leaving it surrounded by two bilayer membranes. During the engulfment process an essential channel apparatus is thought to cross both membranes to create a direct conduit between the mother cell and forespore. At least nine proteins are essential for channel formation, including SpoIIQ under forespore control and the eight SpoIIIA proteins (SpoIIIAA to -AH) under mother cell control. Presumed to form a core channel complex, several of these proteins share similarity with components of Gram-negative bacterial secretion systems, including the type II, III, and IV secretion systems and the flagellum. Based on these similarities it has been suggested that the sporulation channel represents a hybrid, secretion-like transport machinery. Recently, in-depth biochemical and structural characterization of the individual channel components accompanied by studies has further reinforced this model. Here we review and discuss these recent studies and suggest an updated model for the unique sporulation channel apparatus architecture.

  • Citation: Zeytuni N, Strynadka N. 2019. A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective. Microbiol Spectrum 7(1):PSIB-0013-2018. doi:10.1128/microbiolspec.PSIB-0013-2018.

References

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/content/journal/microbiolspec/10.1128/microbiolspec.PSIB-0013-2018
2019-01-25
2019-08-17

Abstract:

Bacteria employ a number of dedicated secretion systems to export proteins to the extracellular environment. Several of these comprise large complexes that assemble in and around the bacterial membrane(s) to form specialized channels through which only selected proteins are actively delivered. Although typically associated with bacterial pathogenicity, a specialized variant of these secretion systems has been proposed to play a central part in bacterial sporulation, a primitive protective process that allows starving cells to form spores that survive in extreme environments. Following asymmetric division, the mother cell engulfs the forespore, leaving it surrounded by two bilayer membranes. During the engulfment process an essential channel apparatus is thought to cross both membranes to create a direct conduit between the mother cell and forespore. At least nine proteins are essential for channel formation, including SpoIIQ under forespore control and the eight SpoIIIA proteins (SpoIIIAA to -AH) under mother cell control. Presumed to form a core channel complex, several of these proteins share similarity with components of Gram-negative bacterial secretion systems, including the type II, III, and IV secretion systems and the flagellum. Based on these similarities it has been suggested that the sporulation channel represents a hybrid, secretion-like transport machinery. Recently, in-depth biochemical and structural characterization of the individual channel components accompanied by studies has further reinforced this model. Here we review and discuss these recent studies and suggest an updated model for the unique sporulation channel apparatus architecture.

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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.

Source: microbiolspec January 2019 vol. 7 no. 1 doi:10.1128/microbiolspec.PSIB-0013-2018
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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. ( 46 ).

Source: microbiolspec January 2019 vol. 7 no. 1 doi:10.1128/microbiolspec.PSIB-0013-2018
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