Skip to main content

Peptidoglycan (Murein) Hydrolases: Unusual Enzymes for Unusual Substrates

  • Chapter
Bacterial Growth and Lysis

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).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Cornett, J.B, Redman, B.E. and Shockman, G.D. (1978) Autolytic defective mutant of Streptococcus faecalis. J. Bacteriol. 133, 631–640.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Fan, D.P. and Beckman, M.M. (1973) Mutant of Bacillus subtilis with a temperaturesensitive autolytic amidase. J. Bacteriol. 14, 798–803.

    Google Scholar 

  • Fein, J.E. and Rogers, H. J. (1976) Autolytic enzyme-deficient mutants of Bacillus subtilis 168. J. Bacteriol. 127, 1427–1442.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ghuysen, J.-M. (1991) Serine β-lactamases and penicillin-binding proteins. Ann. Rev. Microbiol. 45, 37–67.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Hartmann, R., Bock-Hennig, S.B. and Schwarz, U. (1974) Murein hydrolases in the envelope of Escherichia coli. Eur. J. Biochem. 41, 203–208.

    Article  PubMed  CAS  Google Scholar 

  • Herbold, D.R. and Glaser, L. (1975 a) Bacillus subtilis N-acetylmuramic acid L-alanine amidase. J. Biol. Chem. 250, 1676–1682.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Jolliffe, L.K., Doyle, R.J. and Streips, U.N. (1981) Energized membrane and cellular autolysis in Bacillus subtilis. Cell 25, 753–763.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Koyama, T., Yamada, M. and Matsuhashi, M. (1977) Formation of regular packets of Staphylococcus aureus cells. J. Bacteriol. 129, 1518–1523.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kuroda, A. and Sekiguchi, J. (1991) Molecular cloning and sequencing of a major Bacillus subtilis autolysin gene. J. Bacteriol. 173, 7304–7312.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, H.J., Perkins, H.R. and Ward, J.B. (1980) “Microbial Cell Walls and Membranes,” pp. 437–460. Chapman and Hall, New York.

    Book  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Shockman, G.D., Daneo-Moore, L., Cornett, J.B. and Mychajlonka, M. (1979) Does penicillin kill bacteria? Rev. Infect. Dis. 1, 787–796.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Tomasz, A. (1979a) From penicillin-binding proteins to the lysis and death of bacteria: A 1979 view. Rev. Inf. Dis., 1, 434–467.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Walderich, B. and Höltje, J.-V. (1991) Subcellular distribution of the soluble lytic transglycosylase in Escherichia coli. J. Bacteriol. 173, 5668–5676.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer Science+Business Media New York

About this chapter

Cite this chapter

Shockman, G.D., Chu, CP., Kariyama, R., Tepper, L.K., Daneo-Moore, L. (1993). Peptidoglycan (Murein) Hydrolases: Unusual Enzymes for Unusual Substrates. In: de Pedro, M.A., Höltje, JV., Löffelhardt, W. (eds) Bacterial Growth and Lysis. Federation of European Microbiological Societies Symposium Series, vol 65. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9359-8_25

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-9359-8_25

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-9361-1

  • Online ISBN: 978-1-4757-9359-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics