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Staphylococcal Protein Secretion and Envelope Assembly

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  • Authors: Olaf Schneewind1, Dominique M. Missiakas2
  • Editors: Vincent A. Fischetti3, Richard P. Novick4, Joseph J. Ferretti5, Daniel A. Portnoy6, Miriam Braunstein7, Julian I. Rood8
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, University of Chicago, Chicago, IL 60637; 2: Department of Microbiology, University of Chicago, Chicago, IL 60637; 3: The Rockefeller University, New York, NY; 4: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 5: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 6: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 7: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 8: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
  • Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0070-2019
  • Received 10 April 2019 Accepted 24 May 2019 Published 05 July 2019
  • Dominique M. Misiakas, [email protected]
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  • Abstract:

    The highly cross-linked peptidoglycan represents the rigid layer of the bacterial envelope and protects bacteria from osmotic lysis. In Gram-positive bacteria, peptidoglycan also functions as a scaffold for the immobilization of capsular polysaccharide, wall teichoic acid (WTA), and surface proteins. This chapter captures recent development on the assembly of the envelope of including mechanisms accounting for immobilization of molecules to peptidoglycan as well as hydrolysis of peptidoglycan for the specific release of bound molecules, facilitation of protein secretion across the envelope and cell division. Peptidoglycan, WTA and capsular polysaccharide are directly synthesized onto undecaprenol. Surface proteins are anchored by Sortase A, a membrane-embedded transpeptidase that scans secreted polypeptides for the C-terminal LPXTG motif of sorting signals. The resulting acyl enzyme intermediate is resolved by lipid II, the undecaprenol-bound peptidoglycan precursor. While these pathways share membrane diffusible undecaprenol, assembly of these molecules occurs either at the cross-walls or the cell poles. In , the cross-wall represents the site of peptidoglycan synthesis which is eventually split to complete the cell cycle yielding newly divided daughter cells. Peptidoglycan synthesized at the cross-wall is initially devoid of WTA. Conversely, lipoteichoic acid (LTA) synthesis which does not require bactoprenol is seemingly restricted to septal membranes. Similarly, distinguishes two types of surface protein precursors. Polypeptides with canonical signal peptides are deposited at the cell poles, whereas precursors with conserved YSIRK-GXXS motif signal peptides traffic to the cross-wall. A model for protein trafficking in the envelope and uneven distribution of teichoic acids is discussed.

  • Citation: Schneewind O, Missiakas D. 2019. Staphylococcal Protein Secretion and Envelope Assembly. Microbiol Spectrum 7(4):GPP3-0070-2019. doi:10.1128/microbiolspec.GPP3-0070-2019.

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/content/journal/microbiolspec/10.1128/microbiolspec.GPP3-0070-2019
2019-07-05
2019-08-18

Abstract:

The highly cross-linked peptidoglycan represents the rigid layer of the bacterial envelope and protects bacteria from osmotic lysis. In Gram-positive bacteria, peptidoglycan also functions as a scaffold for the immobilization of capsular polysaccharide, wall teichoic acid (WTA), and surface proteins. This chapter captures recent development on the assembly of the envelope of including mechanisms accounting for immobilization of molecules to peptidoglycan as well as hydrolysis of peptidoglycan for the specific release of bound molecules, facilitation of protein secretion across the envelope and cell division. Peptidoglycan, WTA and capsular polysaccharide are directly synthesized onto undecaprenol. Surface proteins are anchored by Sortase A, a membrane-embedded transpeptidase that scans secreted polypeptides for the C-terminal LPXTG motif of sorting signals. The resulting acyl enzyme intermediate is resolved by lipid II, the undecaprenol-bound peptidoglycan precursor. While these pathways share membrane diffusible undecaprenol, assembly of these molecules occurs either at the cross-walls or the cell poles. In , the cross-wall represents the site of peptidoglycan synthesis which is eventually split to complete the cell cycle yielding newly divided daughter cells. Peptidoglycan synthesized at the cross-wall is initially devoid of WTA. Conversely, lipoteichoic acid (LTA) synthesis which does not require bactoprenol is seemingly restricted to septal membranes. Similarly, distinguishes two types of surface protein precursors. Polypeptides with canonical signal peptides are deposited at the cell poles, whereas precursors with conserved YSIRK-GXXS motif signal peptides traffic to the cross-wall. A model for protein trafficking in the envelope and uneven distribution of teichoic acids is discussed.

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Image of FIGURE 1
FIGURE 1

Schematic illustrating cell division, PBP2-mediated synthesis of cross-wall peptidoglycan, LtaS-mediated synthesis of lipoteichoic acid (LTA) in septal membranes, and the trafficking of surface protein precursors with YSIRK-GXXS motif signal peptides (blue circles) to septal membranes. Following translocation, sortase A-mediated cell wall sorting, and incorporation into the cross-wall, the peptidoglycan layer is split and divided cells are separated, exposing cross-wall-incorporated proteins on the bacterial surface. Surface proteins with canonical signal peptides (red circles) are deposited into polar segments of the peptidoglycan layer.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0070-2019
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Image of FIGURE 2
FIGURE 2

Surface protein anchoring to the cell wall of . Primary structure of the precursor for staphylococcal protein A (SpA) with an N-terminal signal peptide, signal peptidase (SpsB) cleavage site, five immunoglobulin binding domains (IgBDs), region X (Xr), LysM domain, and C-terminal LPXTG-motif sorting signal. Cell wall-anchored SpA is tethered to the envelope via an amide bond between the carboxyl-group of its C-terminal threonyl (T in the LPXTG motif) and the amino group of the pentaglycine cross-bridge within peptidoglycan. Released nSpA encompasses murein tetrapeptide-tetraglycyl [-Ala--iGln-(SpA-Gly)-Lys--Ala-Gly] linked to the C-terminal threonyl of the surface protein. Cell wall sorting pathway of surface proteins in . Following Sec-mediated translocation of surface protein precursors across the membrane, sortase A cleaves the LPXTG-motif of the C-terminal sorting signal between the threonyl (T) and the glycyl (G) residues and forms a thioester bond between its active site cysteinyl and the carboxyl-group of the C-terminal threonyl. The sortase acyl-enzyme intermediate is relieved by the nucleophilic attack of lipid II, thereby generating surface protein linked to peptidoglycan precursor, which is subsequently incorporated by penicillin binding protein 2 into the cell wall peptidoglycan. Through the action of murein hydrolases, surface protein is released from the cell wall into the extracellular milieu.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0070-2019
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