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Chapter 11 : Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus

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Abstract:

This chapter reviews the murein structure and biosynthesis and the possible mechanism(s) of enlargement during growth of gram-negative bacteria. Unless otherwise stated, the presented data were obtained in studies with , which is the most extensively studied gram-negative bacterium with respect to murein structure and biosynthesis. The major subunits in the murein of are the disaccharide tetrapeptide monomer and the DD-cross-linked bisdisaccharide tetratetrapeptide dimer. The layered murein cannot be perfect for two reasons. First, compared with the dimensions of the cell, the glycan strands are rather short. Second, the percentage of cross-linked peptides is slightly lower than the theoretical value of 50%. The final steps in murein synthesis take place at the periplasmic side of the cytoplasmic membrane and involve two reactions. First, the murein glycan strands are oligomerized by transglycosylation, and second, the peptide cross-links are formed by transpeptidation. Of the six known lytic transglycosylases of , only one is soluble (Slt70), whereas five are lipoproteins anchored to the outer membrane (MltA, MltB, MltC, MltD, and EmtA) and face into the periplasm. Murein hydrolases are enzymes that cleave covalent bonds in the murein sacculus or in murein fragments. Morphogenesis of seems rather simple with two phases in the cell cycle. Most models have in common that the enlargement of the sacculus is achieved by the insertion of new glycan strands and that both synthesis of new murein and hydrolysis of bonds within the existing sacculus are combined.

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11

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Figures

Image of FIGURE 1
FIGURE 1

(A) A cryo-transmission electron microscopy picture of a frozen-hydrated section of an cell. The murein layer (PG) is embedded in the envelope between the cytoplasmic membrane (PM) and the outer membrane (OM); bar, 200 nm. ( ] with permission.) The other transmission electron microscopy pictures show isolated murein sacculi from (B), (C), and (D). B to D, bar, 500 nm.

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 2
FIGURE 2

Structure of murein from gram-negative bacteria. (A) The murein glycan strands consist of alternating N-acetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc) residues. A 1,6-an-hydroMurNAc residue is present at one chain end. R, peptide. (B) Structures of monomeric, dimeric, and trimeric peptides. There are two types of cross-links (DD and LD). In the murein, the L-Ala residue of the peptide is attached to the lactyl group of the MurNAc residue of the glycan strands. iGlu (iso-glutamate), the γ-carboxyl group of Glu, is linked to the m-Apm residue. (C) The murein of some bacteria contains an -acetyl group (in bold) at C-6 of a fraction of the MurNAc residues. (D) Structure of the covalent linkage between Braun’s lipoprotein (Lpp) and the tripeptide in the murein.

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 3
FIGURE 3

Architecture of murein. (A) The peptides (arrows) protrude helically from the glycan strands. Light grey bar, GlcNAc; dark grey bar, MurNAc. (B) Model for the architecture of a murein layer. The glycan strands are indicated as bold zigzag lines. Arrows indicate the cross-linked peptides in the murein layer plane). The non-cross-linked peptides pointing up and down are shown as dotted lines. A tessera is the smallest unit (pore) formed by two glycan strands and two peptide cross-links. (C) Model of the murein sacculus. The glycan strands (lines) run in the direction perpendicular to the long axis of the cell direction in B), whereas the peptide cross-links (arrows) are in the direction of the long axis (y direction in B). About 70 to 120 glycan strands of average length are required for one circumference, and about 500 to 1,000 glycan strands are arranged in parallel to cover the length of the cell. Most of the surface of the sacculus is made of a single layer. (Reproduced from Holtje [1998] with permission.)

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 4
FIGURE 4

Murein synthesis reaction with lipid II as substrate.(A) The glycan strands are oligomerized by transglycosylation. pyrophosphate; upr, undecaprenyl. (B) The dd-cross-links are formed by transpeptidation by a penicillin-binding protein (PBP). The intermediate peptidyl-enzyme complex is shown. (left) Donor peptide; (right) acceptor peptide; G, GlcNAc; M, MurNAc.

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 5
FIGURE 5

Murein hydrolysis. (A) Cleavage sites of different classes of murein hydrolases in high-molecularweight murein.A, -acetylmuramyl-l-alanine amidase; LT, lytic transglycosylase;dd-EP, dd-endopeptidase;LD-EP, LD-endopeptidase; DD-CP, DD-carboxypeptidase; LD-CP, LD-carboxypeptidase. (B) Cleavage of a murein glycan strand by an exo-specific lytic transglycosylase (LT) with concomitant formation of a 1,6-anhydro bond at the MurNAc residue.

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 6
FIGURE 6

Model of the enlargement of the murein layer proposed by . (A) Hydrolysis of cross-links precedes the insertion of a new glycan strand, connecting new and old material. (B) After some time, connections between two new strands are also made. (Reproduced from Park [1996] with permission.)

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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Image of FIGURE 7
FIGURE 7

Three-for-one growth model proposed by Höltje. A triplet of three new strands is attached to the sacculus and is inserted by the concomitant removal of one old strand (docking strand). During elongation, one strand of the triplet (the primer strand) is preformed (left side). During cell division, all three strands are newly synthesized (right side). Below are shown the hypothetical murein synthesis multienzyme complexes for the enlargement of the sacculus. Complexes active during elongation contain PBP2, and complexes active during cell division contain PBP3. TG, transglycosylase;TP, transpeptidase; EP, endopeptidase; LT, lytic transglycosylase;A, acetylmuramyl-L-alanine amidase. (Reproduced from Höltje [1998] with permission.)

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11
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References

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1. Antignac, A.,, J. C. Rousselle,, A. Namane,, A. Labigne,, M. K. Taha, and, I. G. Boneca. 2003. Detailed structural analysis of the peptidoglycan of the human pathogen Neisseria meningitidis. J. Biol. Chem. 278:3152131528.
2. Barnickel, G.,, H. Labischinski,, H. Bradaczek, and, P. Giesbrecht. 1979. Conformational energy calculation on the peptide part of murein. Eur. J. Biochem. 95:157165.
3. Barnikel, G.,, D. Naumann,, H. Bradaczek,, H. Labischinski, and, P. Giesbrecht. 1983. Computer aided molecular modelling of the three-dimensional structure of bacterial peptidoglycan, p. 6166. In R. Hakenbeck,, J.-V. Holtje, and, H. Labischinski, (ed.), The Target of Penicillin:The Murein Sacculus of Bacterial Cell Walls. Architecture and Growth. de Gruyter, New York, N.Y.
4. Bayer, M. E., 1979. The fusion sites between outer membrane and cytoplasmic membrane of bacteria: their role in membrane assembly and virus infection, p. 167202. In M. Inoue (ed.) Bacterial Outer Membranes. John Wiley & Sons, Inc., New York, N.Y.
5. Bera, A.,, S. Herbert,, A. Jakob,, W. Vollmer, and, F. Götz. 2005. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55:778787.
6. Bernhardt, T. G., and, P. A. de Boer. 2003. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48:11711182.
7. Bernhardt, T. G., and, P. A. de Boer. 2004. Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol. 52:12551269.
8. Braun, V., and, H. Wolff. 1970. The murein-lipoprotein linkage in the cell wall of Escherichia coli. Eur. J. Biochem. 14:387391.
9. Burman, L. G., and, J. T. Park. 1984. Molecular model for elongation of the murein sacculus of Escherichia coli. Proc. Natl. Acad. Sci. USA 81:18441848.
10. Clarke, A. J., and, C. Dupont. 1992. O-acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis. Can. J. Microbiol. 38: 8591.
11. de Jonge, B. L.,, F. B. Wientjes,, I. Jurida,, F. Driehuis,, J. T. Wouters, and, N. Nanninga. 1989. Peptidoglycan synthesis during the cell cycle of Escherichia coli: composition and mode of insertion. J. Bacteriol. 171:57835794.
12. Demchick, P., and, A. L. Koch. 1996. The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J. Bacteriol. 178:768773.
13. de Pedro, M. A.,, J.-V. Höltje, and, W. Löffelhardt (ed.)., 1993. Bacterial Growth and Lysis. Metabolism and Structure of the Bacterial Sacculus. Plenum Press, New York, N.Y.
14. de Pedro, M. A.,, J. C. Quintela,, J.-V. Höltje, and, H. Schwarz. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:28232834.
15. de Pedro, M. A.,, K. D. Young,, J.-V. Höltje, and, H. Schwarz. 2003. Branching of Escherichia coli cells arises from multiple sites of inert peptidoglycan. J. Bacteriol. 185:11471152.
16. Dijkstra, A. J., and, W. Keck. 1996. Peptidoglycan as a barrier to transenvelope transport. J. Bacteriol. 178:55555562.
17. Dougherty, T. J.,, K. Kennedy,, R. E. Kessler, and, M. J. Pucci. 1996. Direct quantitation of the number of individual penicillin-binding proteins per cell in Escherichia coli. J. Bacteriol. 178:61106115.
18. El Ghachi, M.,, A. Derbise,, A. Bouhss, and, D. Mengin-Lecreulx. 2005. Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J. Biol. Chem. 280:1868918695.
19. Ghuysen, J.-M., 1991. Serine beta-lactamases and penicillin-binding proteins. Annu. Rev. Microbiol. 45:3767.
20. Ghuysen, J. M., and, R. Hakenbeck(ed.)., 1994. Bacterial Cell Wall. Elsevier Science B.V., Amsterdam, The Netherlands.
21. Glauner, B., 1988. Separation and quantification of muropeptides with high-performance liquid chromatography. Anal. Biochem. 172:451464.
22. Glauner, B.,, J.-V. Höltje, and, U. Schwarz. 1988. The composition of the murein of Escherichia coli. J. Biol. Chem. 263:1008810095.
23. Goehring, N. W., and, J. Beckwith. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514R526.
24. Goffin, C., and, J.-M. Ghuysen. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:10791093.
25. Goodell, E. W., 1985. Recycling of murein by Escherichia coli. J. Bacteriol. 163:305310.
26. Harz, H.,, K. Burgdorf, and, J.-V. Höltje. 1990. Isolation and separation of the glycan strands from murein of Escherichia coli by reversed phase highperformance liquid chromatography. Anal. Biochem. 190:120128.
27. Heidrich, C.,, M. F. Templin,, A. Ursinus,, M. Merdanovic,, J. Berger,, H. Schwarz,, M. A. de Pedro, and, J.-V. Höltje. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167178.
28. Höltje, J.-V., 1995. From growth to autolysis: the murein hydrolases in Escherichia coli. Arch. Microbiol. 164:243254.
29. Höltje, J.-V., 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181203.
30. Höltje, J.-V.,, D. Mirelman,, N. Sharon, and, U. Schwarz. 1975. Novel type of murein transglycosylase in Escherichia coli. J. Bacteriol. 124:10671076.
31. Jacobs, C.,, J. M. Frere, and, S. Normark. 1997. Cytosolic intermediates for cell wall biosynthesis and degradation control inducible beta-lactam resistance in gram-negative bacteria. Cell 88:823832.
32. Jones, L. J.,, R. Carballido-Lopez, and, J. Errington. 2001. Control of cell shape in bacteria:helical, actin-like filaments in Bacillus subtilis. Cell 104:913922.
33. Joris, B.,, P. Ledent,, O. Dideberg,, E. Fonze,, J. Lamotte-Brasseur,, J. A. Kelly,, J. M. Ghuysen, and, J.-M. Frere. 1991. Comparison of the sequences of class A beta-lactamases and of the secondary structure elements of penicillin-recognizing proteins. Antimicrob. Agents Chemother. 35:22942301.
34. Kellenberger, E., 1990. The ‘Bayer bridges’ confronted with results from improved electron microscopy methods. Mol. Microbiol. 4:697705.
35. Koch, A. L., 1995. Bacterial Growth and Form. Chapman & Hall, New York, N.Y.
36. Koch, A. L., 1998. Orientation of the peptidoglycan chains in the sacculus of Escherichia coli. Res. Microbiol. 149:689–701.
37. Koch, A. L.,, S. L. Lane,, J. A. Miller, and, D. G. Nickens. 1987. Contraction of filaments of Escherichia coli after disruption of cell membrane by detergent. J. Bacteriol. 169:19791984.
38. Koch, A. L., and, S. Woeste. 1992. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174:48114819.
39. Labischinski, H.,, G. Barnickel,, D. Naumann, and, P. Keller. 1985. Conformational and topological aspects of the three-dimensional architecture of bacterial peptidoglycan. Ann. Inst. Pasteur Microbiol. 136A:4550.
40. Labischinski, H.,, E. W. Goodell,, A. Goodell, and, M. L. Hochberg. 1991. Direct proof of a ‘morethan-single-layered’ peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J. Bacteriol. 173:751756.
41. Matias, V. R.,, A. Al-Amoudi,, J. Dubochet, and, T. J. Beveridge. 2003. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185:61126118.
42. Matsuhashi, M.,, M. Wachi, and, F. Ishino. 1990. Machinery for cell growth and division: penicillin-binding proteins and other proteins. Res. Microbiol. 141:89103.
43. Meisel, U.,, J.-V. Holtje, and, W. Vollmer. 2003. Overproduction of inactive variants of the murein synthase PBP1B causes lysis in Escherichia coli. J. Bacteriol. 185:53425348.
44. Nambu, T.,, T. Minamino,, R. M. Macnab, and, K. Kutsukake. 1999. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181:15551561.
45. Nanninga, N., 1998. Morphogenesis of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:110129.
46. Nilsen, T.,, A. S. Gosh,, M. B. Goldberg, and, K. D. Young. 2004. Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli. Mol. Microbiol. 52:10451054.
47. Park, J. T., 1993. Turnover and recycling in oligopeptide permease-negative strains of Escherichia coli: indirect evidence for an alternative permease system and for a monolayered sacculus. J. Bacteriol. 175:711.
48. Park, J. T., 1996. The murein sacculus, p. 4857. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter, and, H. E. Umbarger, (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed., vol. 1. ASM Press,Washington, D.C.
49. Quintela, J. C.,, M. Caparros, and, M. A. de Pedro. 1995. Variability of peptidoglycan structural parameters in gram-negative bacteria. FEMS Microbiol. Lett. 125:95100.
50. Romeis, T., and, J.-V. Höltje. 1994. Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J. Biol. Chem. 269:2160321607.
51. Schleifer, K. H., and, O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407477.
52. Terrak, M.,, T. K. Ghosh,, J. van Heijenoort,, J. Van Beeumen,, M. Lampilas,, J. Aszodi,, J. A. Ayala,, J.-M. Ghuysen, and, M. Nguyen-Disteche. 1999. The catalytic, glycosyl transferase and acyl transferase modules of the cell wall peptidoglycanpolymerizing penicillin-binding protein 1b of Escherichia coli. italic>Mol. Microbiol. 34:350364.
53. Tokuda, H., and, S. Matsuyama. 2004. Sorting of lipoproteins to the outer membrane in E. coli. Biochim. Biophys. Acta 1693:513.
54. Uehara, T.,, K. Suefuji,, N. Valbuena,, B. Meehan,, M. Donegan, and, J. T. Park. 2005. Recycling of the anhydro-N-acetylmuramic acid derived from cell wall murein involves a two-step conversion to N-acetylglucosamine-phosphate. J. Bacteriol. 187:36433649.
55. van Heijenoort, J., 1998. Assembly of the monomer unit of bacterial peptidoglycan. Cell. Mol. Life Sci. 54:300304.
56. Varma, A., and, K. D. Young. 2004. FtsZ collaborates with penicillin-binding proteins to generate bacterial shape in Escherichia coli. J. Bacteriol. 186:67886774.
57. Vollmer, W., and, J.-V. Höltje. 2001. Morphogenesis of Escherichia coli. Curr. Opin. Microbiol. 4:625633.
58. Vollmer, W., and, J.-V. Holtje. 2004. The architecture of the murein (peptidoglycan) in gram-negative bacteria: vertical scaffold or horizontal layer(s)? J. Bacteriol. 186:59785987.
59. Vollmer, W.,, M. von Rechenberg, and, J.-V. Höltje. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274:67266734.
60. Weidel, W., and, H. Pelzer. 1964. Bagshaped macromolecules–a new outlook on bacterial cell walls. Adv. Enzymol. 26:193232.
61. Weiss, D. S., 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588597.
62. Wientjes, F. B.,, C. L. Woldringh, and, N. Nanninga. 1991. Amount of peptidoglycan in cell walls of gram-negative bacteria. J. Bacteriol. 173:76847691.
63. Woldringh, C.,, P. Huls,, E. Pas,, G. H. Brakenhoff, and, N. Nanninga. 1987. Topography of peptidoglycan synthesis during elongation and polar cap formation in a cell division mutant of Escherichia coli MC43100. J. Gen. Microbiol. 133:575586.
64. Yao, X.,, M. Jericho,, D. Pink, and, T. J. Beveridge. 1999. Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181:68656875.
65. Young, K. D., 2003. Bacterial shape. Mol. Microbiol. 49:571580.

Tables

Generic image for table
TABLE 1

The periplasmic murein synthases and hydrolases in

Citation: Vollmer W. 2007. Structure and Biosynthesis of the Murein (Peptidoglycan) Sacculus, p 198-213. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch11

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