Peptidoglycan (Murein) Hydrolases: Unusual Enzymes for Unusual Substrates

  • Gerald D. Shockman
  • Chien-Peng Chu
  • Reiko Kariyama
  • Lori K. Tepper
  • Lolita Daneo-Moore
Part of the Federation of European Microbiological Societies Symposium Series book series (FEMS, volume 65)

Abstract

A broad variety of both Gram-positive and Gram-negative bacteria have been shown to have the ability to dissolve themselves (autolyze), particularly under “adverse” conditions (see Ghuysen and Shockman, 1973; Daneo-Moore and Shockman, 1977; Rogers et al., 1980; Shockman and Barrett, 1983; Doyle and Koch, 1987; Höltje and Tuomanen, 1991, for reviews). This process is now known to be initiated by the action of endogenous enzymes that hydrolyze specific bonds in the insoluble, osmotically protective, shape-maintaining and essential, peptidoglycan (murein) polymer of the bacterial cell wall. Hydrolysis of a sufficient number of bonds in a restricted area of the two- or three-dimensional peptidoglycan network, or a larger number of bonds in a broader area of the wall, creates a weak spot (or a generalized weakness in the structure), so that the wall can no longer protect the protoplast from its own internal osmotic pressure, so that the protoplast then explodes out through the weakened structure. Endogenous enzymes are now known that can hydrolyze virtually every bond in the peptidoglycan including: (i) glycosidases and transglycosidases, such as N-acetylmuramoylhydrolases (muramidases) and N-acetylglucosaminidases, (ii) N-acetylmuramoyl-L-alanine amidases, and (iii) various peptidases and transpeptidases, including DD- and LD-carboxypeptidases (Rogers et al., 1980).

Keywords

Muramidase Activity Cell Wall Peptidoglycan Derive Amino Acid Sequence Wall Teichoic Acid Peptidoglycan Hydrolase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barrett, J.F. and Shockman, G.D. (1984) Isolation and characterization of soluble peptidoglycan from, several strains of Streptococcus faecium. J. Bacteriol. 159, 511–519.PubMedGoogle Scholar
  2. Barrett, J.F, Dolinger, D.L., Schramm, V.L., and Shockman, G.D. (1984a) The mechanism of soluble peptidoglycan hydrolysis by an autolytic muramidase. A processive exodisaccharidase. J. Biol. Chem. 259, 11818–11827.Google Scholar
  3. Barrett, J.F, Schramm, V.L. and Shockman, G.D. (1984) Hydrolysis of soluble, linear, un-cross-linked peptidoglycans by endogenous bacterial N-acetylmuramoylhydrolases. J. Bacteriol. 159, 520–526.PubMedGoogle Scholar
  4. Beck, B. and Park, J.T. (1976) Activity of three murein hydrolases during the cell division cycle of Escherichia coli as measured in toluene-treated cells. J. Bacteriol. 126, 1250–1260.PubMedGoogle Scholar
  5. Beliveau, C, Potvin, C, Trudel, J, Asselin, A. and Bellemare, G. (1991) Cloning, sequencing, and expression in Escherichia coli of a Streptococcus faecalis autolysin. J. Bacteriol. 173, 5619–5623.PubMedGoogle Scholar
  6. Biavasco, F, Pruzzo, C. and Thomas, C. (1988) Cloning and expression of the Staphylococcus aureus glucosaminidase in Escherichia coli. FEMS Microbiol. Lett. 49, 137–142.CrossRefGoogle Scholar
  7. Chatterjee, A.N., Wong, W, Young, F.E. and Gilpin, R.W. (1976) Isolation and characterization of a mutant of Staphylococcus aureus deficient in autolytic activity. J. Bacteriol. 125, 961–967.PubMedGoogle Scholar
  8. Chu, C.-P, Kariyama, R, Daneo-Moore, L. and Shockman, G.D. (1992) Cloning and sequence analysis of the muramidase-2 gene from Enterococcus hirae. J. Bacteriol. 174, 1619–1625.PubMedGoogle Scholar
  9. Cleveland, R. F, Höltje, J.-V, Wicken, A. J, Tomasz, A, Daneo-Moore, L. and Shockman, G.D. (1975) Inhibition of bacterial wall lysins by lipoteichoic acids and related compounds. Biochem. Biophys. Res. Commun. 67, 1128–1135.PubMedCrossRefGoogle Scholar
  10. Cleveland, R. F, Wicken, A. J, Daneo-Moore, L. and Shockman, G.D. (1976) Inhibition of wall autolysis in Streptococcus faecalis by lipoteichoic acid and lipids. J. Bacteriol. 126, 192–197.PubMedGoogle Scholar
  11. Conover, M.J, Thompson, J.S. and Shockman, G.D. (1966) Autolytic enzyme of Streptococcus faecalis: release of soluble enzyme from cell walls. Biochem. Biophys. Res. Commun. 23, 713–719.PubMedCrossRefGoogle Scholar
  12. Cornett, J.B, Redman, B.E. and Shockman, G.D. (1978) Autolytic defective mutant of Streptococcus faecalis. J. Bacteriol. 133, 631–640.PubMedGoogle Scholar
  13. Coyette, J, Perkins, H.R, Polacheck, I, Shockman, G.D. and Ghuysen, J.-M. (1974) Membrane-bound DD-carboxypeptidase and LD-transpeptidase of Streptococcus faecalis ATCC 9790. Eur. J. Biochem. 44, 459–468.PubMedCrossRefGoogle Scholar
  14. Coyette, J., Ghuysen, J.-M., Binot, F., Adriaens, P., Meesschaert, B. and Vanderhaeghe, H. (1977) Interactions between β-lactam antibiotics and isolated membranes of Streptococcus faecalis ATCC 9790. Eur. J. Biochem. 75, 231–239.PubMedCrossRefGoogle Scholar
  15. Croux, C. and García, J.-L. (1991) Sequence of the lye gene encoding the autolytic lysozyme of Clostridium acetobutylicum ATCC 824: comparison with other lytic enzymes. Gene 104, 25–31.PubMedCrossRefGoogle Scholar
  16. Daneo-Moore, L. and Shockman, G.D. (1977) The Bacterial Cell Surface in Growth and Division, In “Cell Surface Reviews, vol. 4. The Synthesis, Assembly, and Turnover of Cell Surface Components” (Poste, G. and Nicolson, G.L., Eds.), pp. 597–715. Elsevier/North Holland, Amsterdam.Google Scholar
  17. Dolinger, D.L., Schramm, V.L. and Shockman, G.D. (1988) Covalent modification of the β-l,4-N-acetylmuramoylhydrolase of Streptococcus faecium with 5-mercaptouridine monophosphate. Proc. Natl. Acad. Sci. USA 85, 6667–6671.PubMedCrossRefGoogle Scholar
  18. Dolinger, D.L., Daneo-Moore, L. and Shockman, G.D. (1989) The second peptidoglycan hydrolase of Streptococcus faecium ATCC 9790 covalently binds penicillin. J. Bacteriol. 171, 4355–4361.PubMedGoogle Scholar
  19. Doyle, R.J. and Koch, A.L. (1987) The functions of autolysins in the growth and division of Bacillus subtilis. Crit. Rev. Microbiol. 15, 169–222.PubMedCrossRefGoogle Scholar
  20. El Kharroubi, A., Jacques, P., Piras, G., Van Beeumen, J., Coyette, J. and Ghuysen, J.-M. (1991) The Enterococcus hirae R40 penicillin-binding protein 5 and the methicillin-resistant Staphylococcus aureus penicillin-binding protein 2′ are similar. Biochem. J. 280, 463–469.PubMedGoogle Scholar
  21. Fan, D.P. and Beckman, M.M. (1973) Mutant of Bacillus subtilis with a temperaturesensitive autolytic amidase. J. Bacteriol. 14, 798–803.Google Scholar
  22. Fein, J.E. and Rogers, H. J. (1976) Autolytic enzyme-deficient mutants of Bacillus subtilis 168. J. Bacteriol. 127, 1427–1442.PubMedGoogle Scholar
  23. Foster, S.J. (1991) Cloning, expression, sequence analysis and biochemical characterization of an autolytic amidase of Bacillus subtilis 168 trpC2. J. Gen. Microbiol. 137, 1987–1998.PubMedCrossRefGoogle Scholar
  24. García, E., García, J.L., Ronda, C, García, P. and Lopez, R. (1985) Cloning and expression of the pneumococcal autolysin gene of Escherichia coli. Mol. Gen. Genet. 201, 225–230.PubMedCrossRefGoogle Scholar
  25. García, J.L., Sanchez-Puelles, J.M., García, P., Lopez, R., Ronda, C. and García, E. (1986) Molecular characterization of an autolysin-defective mutant of Streptococcus pneumoniae. Biochem. Biophys. Res. Comm. 137, 614–619.PubMedCrossRefGoogle Scholar
  26. García, E., García, J.L., García, P., Arraras, A., Sanchez-Puelles, J.M. and Lopez, R. (1988) Molecular evolution of lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Proc. Natl. Acad. Sci. USA 85, 914–918.PubMedCrossRefGoogle Scholar
  27. García, P., García, J.L, García, E., Sanchez-Puelles, J.M. and Lopez, R. (1990) Modular organization of the lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Gene 86, 81–88.PubMedCrossRefGoogle Scholar
  28. Garvey, K.J., Saedi, M.S. and Ito, J. (1986). Nucleotide sequence of Bacillus phage φ29 genes 14 and 15: homology of gene 15 with other phage lysozymes. Nucleic Acid Res. 14, 10001–10008.PubMedCrossRefGoogle Scholar
  29. Ghuysen, J.-M. (1991) Serine β-lactamases and penicillin-binding proteins. Ann. Rev. Microbiol. 45, 37–67.CrossRefGoogle Scholar
  30. Ghuysen, J.-M. and Shockman, G.D. (1973) Biosynthesis of Peptidoglycan, in “Bacterial Membranes and Walls” (Leive, L., Ed.), pp. 37–130. Marcel Dekker, New York.Google Scholar
  31. Hakenbeck, R. and Messer, W. (1974) Activity of murein hydrolases and membrane synthesis in synchronized Escherichia coli B/r. Ann. Microbiol. Inst. Pasteur 125B, 163–166s.Google Scholar
  32. Hartmann, R., Bock-Hennig, S.B. and Schwarz, U. (1974) Murein hydrolases in the envelope of Escherichia coli. Eur. J. Biochem. 41, 203–208.PubMedCrossRefGoogle Scholar
  33. Herbold, D.R. and Glaser, L. (1975 a) Bacillus subtilis N-acetylmuramic acid L-alanine amidase. J. Biol. Chem. 250, 1676–1682.PubMedGoogle Scholar
  34. Herbold, D.R. and Glaser, L. (1915b) Interaction of Af-acetylmuramic acid L-alanine amidase with cell wall polymers. J. Biol. Chem. 250, 7231–7238.Google Scholar
  35. Higgins, M. L., Pooley, H. M. and Shockman, G.D. (1970) Site of initiation of cellular autolysis in Streptococcus faecalis as seen by electron microscopy. J. Bacteriol. 103, 504–512.PubMedGoogle Scholar
  36. Hinks, R. P., Daneo-Moore, L. and Shockman, G.D. (1978) Cellular autolytic activity in synchronized populations of Streptococcus faecium. J. Bacteriol. 133, 822–829.PubMedGoogle Scholar
  37. Höltje, J.-V. and Tomasz, A. (1975) Lipoteichoic acid: A specific inhibitor of autolysin activity in Pneumococcus. Proc. Natl. Acad. Sci. USA 72, 1690–1694.PubMedCrossRefGoogle Scholar
  38. Höltje, J.-V. and Tuomanen, E.I. (1991) The murein hydrolases of Escherichia coli: properties, functions, and impact on the course of infections in vivo. J. Gen. Microbiol. 137, 441–454.PubMedCrossRefGoogle Scholar
  39. Jayaswal, R.K., Lee, Y.-I. and Wilkinson, B.J. (1990) Cloning and expression of a Staphylococcus aureus gene encoding a peptidoglycan hydrolase activity. J. Bacteriol. 172, 5783–5788.PubMedGoogle Scholar
  40. Jolliffe, L.K., Doyle, R.J. and Streips, U.N. (1981) Energized membrane and cellular autolysis in Bacillus subtilis. Cell 25, 753–763.PubMedCrossRefGoogle Scholar
  41. Jones, C.J., Homma, M. and Macnab, R.M. (1989) L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: Gene sequences and deduced protein sequences. J. Bacteriol. 171, 3890–3900.PubMedGoogle Scholar
  42. Joris, B., Englebert, S., Chu, C.-P., Kariyama, R., Daneo-Moore, L., Shockman, G.D. and Ghuysen, J.-M. (1992) Modular design of the Enterococcus hirae muramidase2 and Streptococcus faecalis autolysin. FEMS Microbiol. Lett., in press.Google Scholar
  43. Joseph, R. and Shockman, G.D. (1976) Autolytic formation of protoplasts (autoplasts) of Streptococcus faecalis: location of active and latent autolysin. J. Bacteriol. 127, 1482–1493.PubMedGoogle Scholar
  44. Kariyama, R. and Shockman, G.D. (1992) Extracellular and cellular distribution of muramidase-2 and muramidase-1 of Enterococcus hirae ATCC 9790. J. Bacteriol., in press.Google Scholar
  45. Kawamura, T. and Shockman, G.D. (1983a) Evidence for the presence of a second peptidoglycan hydrolase in Streptococcus faecium. FEMS Microbiol. Lett. 19, 65–69.CrossRefGoogle Scholar
  46. Kawamura, T. and Shockman, G.D. (1983b) Purification and some properties of the endogenous, autolytic N-acetylmuramoylhydrolase of Streptococcus faecium, a bacterial glycoenzyme. J. Biol. Chem. 258, 9514–9521.PubMedGoogle Scholar
  47. Köhler, S., Leimeister-Wächter, L., Chakraborty, T., Lottspeich, F. and Goebel, W. (1990) The gene coding for protein p60 of Listeria monocytogenes and its use as a specific probe for Listeria monocytogenes. Inf. Immun. 58, 1943–1950.Google Scholar
  48. Koyama, T., Yamada, M. and Matsuhashi, M. (1977) Formation of regular packets of Staphylococcus aureus cells. J. Bacteriol. 129, 1518–1523.PubMedGoogle Scholar
  49. Kuroda, A. and Sekiguchi, J. (1990) Cloning, sequencing, and genetic mapping of a Bacillus subtilis cell wall hydrolase gene. J. Gen. Microbiol. 136, 2209–2216.PubMedCrossRefGoogle Scholar
  50. Kuroda, A. and Sekiguchi, J. (1991) Molecular cloning and sequencing of a major Bacillus subtilis autolysin gene. J. Bacteriol. 173, 7304–7312.PubMedGoogle Scholar
  51. Nakagawa, J. and Matsuhashi, M. (1982) Molecular divergence of a major peptidoglycan synthetase with transglycosylase-transpeptidase activities in Escherichia coli—penicillin-binding protein IBs. Biochem. Biophys. Res. Commun. 105, 1–11.CrossRefGoogle Scholar
  52. Nakagawa, J., Tamake, S., Tomioka, S. and Matsuhashi, M. (1984) Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. J. Biol. Chem. 259, 13937–13946.PubMedGoogle Scholar
  53. Paces, V., Uleek, C. and Urbanek, D. (1986) Nucleotide sequence of the late region of Bacillus subtilis phage PZA, a close relative of phi 29. Gene 44, 107–114.PubMedCrossRefGoogle Scholar
  54. Pooley, H.M. and Shockman, G.D. (1969) Relationship between the latent form and the active form of the autolytic enzyme of Streptococcus faecalis. J. Bacteriol. 100, 617–624.PubMedGoogle Scholar
  55. Pooley, H.M. and Shockman, G.D. (1970) Relationship between the location of autolysin, cell wall synthesis, and the development of resistance to cellular autolysis in Streptococcus faecalis after inhibition of protein synthesis. J. Bacteriol. 103, 457–466.PubMedGoogle Scholar
  56. Pooley, H.M., Shockman, G.D., Higgins, M.L. and Porres-Juan, J. (1972) Some properties of two autolytic-defective mutants of Streptococcus faecalis ATCC 9790. J. Bacteriol. 109, 423–431.PubMedGoogle Scholar
  57. Potvin, C, Leclerc, D., Tremblay, G., Asselin, A. and Bellemare, G. (1988) Cloning, sequencing and expression of a Bacillus bacteriolytic enzyme in Escherichia coli. Mol. Gen Genet 214, 241–248.PubMedCrossRefGoogle Scholar
  58. Rogers, H.J., Perkins, H.R. and Ward, J.B. (1980) “Microbial Cell Walls and Membranes,” pp. 437–460. Chapman and Hall, New York.CrossRefGoogle Scholar
  59. Saedi, M.S., Garvey, K.J. and Ito, J. (1987) Cloning and purification of a unique lysozyme produced by Bacillus phage 029. Proc. Natl. Acad. Sci. USA 84, 955–958.PubMedCrossRefGoogle Scholar
  60. Sekiguchi, J., Ezaki, B., Kodama, K. and Akamatsu, T. (1988) Molecular cloning of a gene affecting the autolysin level and flagellation in Bacillus subtilis. J. Gen. Microbiol. 134, 1611–1621.PubMedGoogle Scholar
  61. Shockman, G.D. (1965) Symposium on the fine structure and replication of bacteria and their parts. IV. Unbalanced cell-wall synthesis: autolysis and cell-wall thickening. Bacteriol. Rev. 29, 345–358.Google Scholar
  62. Shockman, G.D. and Barrett, J.F. (1983) Structure, function, and Assembly of cell walls of Gram-positive bacteria. Ann. Rev. Microbiol. 37, 501–527.CrossRefGoogle Scholar
  63. Shockman, G.D. and Cheney, M.C. (1969) Autolytic enzyme system of Streptococcus faecalis. V. Nature of the autolysin-cell wall complex and its relationship to properties of the autolytic enzyme of Streptococcus faecalis. J. Bacteriol. 98,1199–1207.PubMedGoogle Scholar
  64. Shockman, G.D., Thompson, J.S. and Conover, M.J. (1967) The autolytic enzyme system of Streptococcus faecalis. II. Partial characterization of the autolysin and its substrate. Biochemistry 6, 1054–1065.Google Scholar
  65. Shockman, G.D., Daneo-Moore, L. and Higgins, M.L. (1974) Problems of cell wall and membrane growth, enlargement and division. Ann. N.Y. Acad. Sci. 235, 161–197.PubMedCrossRefGoogle Scholar
  66. Shockman, G.D., Daneo-Moore, L., Cornett, J.B. and Mychajlonka, M. (1979) Does penicillin kill bacteria? Rev. Infect. Dis. 1, 787–796.CrossRefGoogle Scholar
  67. Shockman, G.D, Daneo-Moore, L., McDowell, T.D. and Wong, W. (1982) The Relationship Between Inhibition of Cell Wall Synthesis and Bacterial Lethality, in “The Chemistry and Biology of β-Lactam Antibiotics” (Gorman, M. and Morin, R.B, Eds.), vol. 3, pp. 303–338. Academic Press, New York.Google Scholar
  68. Shockman, G.D, Kawamura, T, Barrett, J.F. and Dolinger, D. (1983) The Autolytic System of Streptococcus faecium, in “The Target of Penicillin — International FEMS Symposium on the Murein Sacculus of Bacterial Cell Walls — Architecture and Growth” (Hakenbeck, R, Höltje, J.-V. and Labischinski, H, Eds.), pp. 165–172. W. de Gruyter & Co, Berlin, New York.Google Scholar
  69. Shockman, G.D., Dolinger, D.L. and Daneo-Moore, L. (1988) The Autolytic Peptidoglycan Hydrolases of Streptococcus faecium: Two Unusual Enzymes, in “Antibiotic Inhibition of Bacteriai Cell Wall Assembly and Function” (Actor, P., Daneo-Moore, L., Higgins, M.L., Salton, M.R.J. and Shockman, G.D., Eds.), pp. 195–210. American Society for Microbiology, Washington, DC.Google Scholar
  70. Shungu, D.L., Cornett, J.B. and Shockman, G.D. (1979) Morphological and physiological study of autolytic-defective Streptococcus faecium strains. J. Bacteriol. 138, 598–608.PubMedGoogle Scholar
  71. Tomasz, A. (1979a) From penicillin-binding proteins to the lysis and death of bacteria: A 1979 view. Rev. Inf. Dis., 1, 434–467.CrossRefGoogle Scholar
  72. Tomasz, A. (1979) The mechanism of the irreversible antimicrobial effects of penicillins: How the beta-lactam antibiotics kill and lyse bacteria. Ann. Rev. Microbiol. 33, 113–37.CrossRefGoogle Scholar
  73. Uhlen, M., Guss, B., Wilsson, B, Gatenbeck, S, Phillipson, L. and Linberg, M. (1984) Complete sequence of the staphylococcal gene encoding protein A. J. Biol. Chem. 259, 1695–1702.PubMedGoogle Scholar
  74. Walderich, B. and Höltje, J.-V. (1991) Subcellular distribution of the soluble lytic transglycosylase in Escherichia coli. J. Bacteriol. 173, 5668–5676.PubMedGoogle Scholar
  75. Wang, X., Wilkinson, B.J. and Jayaswal, R.K. (1991) Sequence analysis of a Staphylococcus aureus gene encoding ä peptidoglycan hydrolase activity. Gene 102, 105–109.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Gerald D. Shockman
    • 1
  • Chien-Peng Chu
    • 1
  • Reiko Kariyama
    • 1
  • Lori K. Tepper
    • 1
  • Lolita Daneo-Moore
    • 1
  1. 1.Department of Microbiology and ImmunologyTemple University School of MedicinePhiladelphiaUSA

Personalised recommendations