1887

Abstract

The gene (renamed ) of IL1403 was shown to encode a peptidoglycan -acetylglucosamine deacetylase. Inactivation of in led to fully acetylated peptidoglycan, whereas cloning of on a multicopy plasmid vector resulted in an increased degree of peptidoglycan deacetylation, as shown by analysis of peptidoglycan constituent muropeptides. An increased amount of -unsubstituted glucosamine residues in peptidoglycan resulted in a reduction of the rate of autolysis of cells. The activity of the major autolysin AcmA was tested on cells or peptidoglycan with different degrees of de--acetylation. Deacetylated peptidoglycan exhibited decreased susceptibility to AcmA hydrolysis. This reduced susceptibility to AcmA did not result from reduced AcmA binding to peptidoglycan with an increasing degree of de--acetylation. In conclusion, enzymic -acetylglucosamine deacetylation protects peptidoglycan from hydrolysis by the major autolysin AcmA in cells, and this leads to decreased cellular autolysis.

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2007-10-01
2019-10-15
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References

  1. Atrih, A., Bacher, G., Allmaier, G., Williamson, M. P. & Foster, S. J. ( 1999; ). Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 181, 3956–3966.
    [Google Scholar]
  2. Blair, D. E., Schuttelkopf, A. W., MacRae, J. I. & van Aalten, D. M. ( 2005; ). Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proc Natl Acad Sci U S A 102, 15429–15434.[CrossRef]
    [Google Scholar]
  3. Boneca, I. G., Dussurget, O., Cabanes, D., Nahori, M. A., Sousa, S., Lecuit, M., Psylinakis, E., Bouriotis, V., Hugot, J. P. & other authors ( 2007; ). A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci U S A 104, 997–1002.[CrossRef]
    [Google Scholar]
  4. Bosma, T., Kanninga, R., Neef, J., Audouy, S. A., van Roosmalen, M. L., Steen, A., Buist, G., Kok, J., Kuipers, O. P. & other authors ( 2006; ). Novel surface display system for proteins on non-genetically modified Gram-positive bacteria. Appl Environ Microbiol 72, 880–889.[CrossRef]
    [Google Scholar]
  5. Buist, G., Kok, J., Leenhouts, K. J., Dabrowska, M., Venema, G. & Haandrikman, A. J. ( 1995; ). Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J Bacteriol 177, 1554–1563.
    [Google Scholar]
  6. Buist, G., Venema, G. & Kok, J. ( 1998; ). Autolysis of Lactococcus lactis is influenced by proteolysis. J Bacteriol 180, 5947–5953.
    [Google Scholar]
  7. Calamita, H. G., Ehringer, W. D., Koch, A. L. & Doyle, R. J. ( 2001; ). Evidence that the cell wall of Bacillus subtilis is protonated during respiration. Proc Natl Acad Sci U S A 98, 15260–15263.[CrossRef]
    [Google Scholar]
  8. Chaurand, P., Luetzenkirchen, F. & Spengler, B. ( 1999; ). Peptide and protein identification by matrix-assisted laser desorption ionization (MALDI) and MALDI-post-source decay time-of-flight mass spectrometry. J Am Soc Mass Spectrom 10, 91–103.[CrossRef]
    [Google Scholar]
  9. Chich, J. F., Rigolet, P., Nardi, M., Gripon, J. C., Ribadeau-Dumas, B. & Brunie, S. ( 1995; ). Purification, crystallization, and preliminary X-ray analysis of PepX, an X-prolyl dipeptidyl aminopeptidase from Lactococcus lactis. Proteins 23, 278–281.[CrossRef]
    [Google Scholar]
  10. Chopin, A., Chopin, M. C., Moillo-Batt, A. & Langella, P. ( 1984; ). Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid 11, 260–263.[CrossRef]
    [Google Scholar]
  11. Chopin, A., Bolotin, A., Sorokin, A., Ehrlich, S. D. & Chopin, M. ( 2001; ). Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res 29, 644–651.[CrossRef]
    [Google Scholar]
  12. Cornett, J. B. & Shockman, G. D. ( 1978; ). Cellular lysis of Streptococcus faecalis induced with Triton X-100. J Bacteriol 135, 153–160.
    [Google Scholar]
  13. Courtin, P., Miranda, G., Guillot, A., Wessner, F., Mezange, C., Domakova, E., Kulakauskas, S. & Chapot-Chartier, M. P. ( 2006; ). Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an l,d-carboxypeptidase involved in peptidoglycan maturation. J Bacteriol 188, 5293–5298.[CrossRef]
    [Google Scholar]
  14. Coutinho, P. M. & Henrissat, B. ( 1999; ). Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering, pp. 3–12. Edited by H. J. Gilbert, G. Davies, B. Henrissat & B. Svensson. Cambridge: The Royal Society of Chemistry.
  15. Croux, C., Canard, B., Goma, G. & Soucaille, P. ( 1992; ). Purification and characterization of an extracellular muramidase of Clostridium acetobutylicum ATCC 824 that acts on non-N-acetylated peptidoglycan. Appl Environ Microbiol 58, 1075–1081.
    [Google Scholar]
  16. Delcour, J., Ferain, T., Deghorain, M., Palumbo, E. & Hols, P. ( 1999; ). The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 76, 159–184.[CrossRef]
    [Google Scholar]
  17. Grangette, C., Muller-Alouf, H., Hols, P., Goudercourt, D., Delcour, J., Turneer, M. & Mercenier, A. ( 2004; ). Enhanced mucosal delivery of antigen with cell wall mutants of lactic acid bacteria. Infect Immun 72, 2731–2737.[CrossRef]
    [Google Scholar]
  18. Guedon, E., Serror, P., Ehrlich, S. D., Renault, P. & Delorme, C. ( 2001; ). Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol Microbiol 40, 1227–1239.[CrossRef]
    [Google Scholar]
  19. Guillot, A., Gitton, C., Anglade, P. & Mistou, M. Y. ( 2003; ). Proteomic analysis of Lactococcus lactis, a lactic acid bacterium. Proteomics 3, 337–354.[CrossRef]
    [Google Scholar]
  20. Hayashi, H., Araki, Y. & Ito, E. ( 1973; ). Occurrence of glucosamine residues with free amino groups in cell wall peptidoglycan from bacilli as a factor responsible for resistance to lysozyme. J Bacteriol 113, 592–598.
    [Google Scholar]
  21. Holo, H. & Nes, I. F. ( 1989; ). High-frequency transformation by electroporation of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 55, 3119–3123.
    [Google Scholar]
  22. Huard, C., Miranda, G., Wessner, F., Bolotin, A., Hansen, J., Foster, S. J. & Chapot-Chartier, M. P. ( 2003; ). Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology 149, 695–705.[CrossRef]
    [Google Scholar]
  23. Huard, C., Miranda, G., Redko, Y., Wessner, F., Foster, S. J. & Chapot-Chartier, M. P. ( 2004; ). Analysis of the peptidoglycan hydrolase complement of Lactococcus lactis: identification of a third N-acetylglucosaminidase, AcmC. Appl Environ Microbiol 70, 3493–3499.[CrossRef]
    [Google Scholar]
  24. Kawagishi, S., Araki, Y. & Ito, E. ( 1980; ). Bacillus cereus autolytic endoglucosaminidase active on cell wall peptidoglycan with N-unsubstituted glucosamine residues. J Bacteriol 141, 137–143.
    [Google Scholar]
  25. Kemper, M. A., Urrutia, M. M., Beveridge, T. J., Koch, A. L. & Doyle, R. J. ( 1993; ). Proton motive force may regulate cell wall-associated enzymes of Bacillus subtilis. J Bacteriol 175, 5690–5696.
    [Google Scholar]
  26. Lazarevic, V., Margot, P., Soldo, B. & Karamata, D. ( 1992; ). Sequencing and analysis of the Bacillus subtilis lytRABC divergon: a regulatory unit encompassing the structural genes of the N-acetylmuramoyl-l-alanine amidase and its modifier. J Gen Microbiol 138, 1949–1961.[CrossRef]
    [Google Scholar]
  27. Lortal, S. & Chapot-Chartier, M. P. ( 2005; ). Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int Dairy J 15, 857–871.[CrossRef]
    [Google Scholar]
  28. Nouaille, S., Ribeiro, L. A., Miyoshi, A., Pontes, D., Le Loir, Y., Oliveira, S. C., Langella, P. & Azevedo, V. ( 2003; ). Heterologous protein production and delivery systems for Lactococcus lactis. Genet Mol Res 2, 102–111.
    [Google Scholar]
  29. Palumbo, E., Deghorain, M., Cocconcelli, P. S., Kleerebezem, M., Geyer, A., Hartung, T., Morath, S. & Hols, P. ( 2006; ). d-Alanyl ester depletion of teichoic acids in Lactobacillus plantarum results in a major modification of lipoteichoic acid composition and cell wall perforations at the septum mediated by the Acm2 autolysin. J Bacteriol 188, 3709–3715.[CrossRef]
    [Google Scholar]
  30. Pfeffer, J. M., Strating, H., Weadge, J. T. & Clarke, A. J. ( 2006; ). Peptidoglycan O- acetylation and autolysin profile of Enterococcus faecalis in the viable but nonculturable state. J Bacteriol 188, 902–908.[CrossRef]
    [Google Scholar]
  31. Poquet, I., Saint, V., Seznec, E., Simoes, N., Bolotin, A. & Gruss, A. ( 2000; ). HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol Microbiol 35, 1042–1051.[CrossRef]
    [Google Scholar]
  32. Psylinakis, E., Boneca, I. G., Mavromatis, K., Deli, A., Hayhurst, E., Foster, S. J., Varum, K. M. & Bouriotis, V. ( 2005; ). Peptidoglycan N-acetylglucosamine deacetylases from Bacillus cereus, highly conserved proteins in Bacillus anthracis. J Biol Chem 280, 30856–30863.[CrossRef]
    [Google Scholar]
  33. Renault, P., Corthier, G., Goupil, N., Delorme, C. & Ehrlich, S. D. ( 1996; ). Plasmid vectors for Gram-positive bacteria switching from high to low copy number. Gene 183, 175–182.[CrossRef]
    [Google Scholar]
  34. Redko, Y., Courtin, P., Mézange, C., Huard, C. & Chapot-Chartier, M.-P. ( 2007; ). Lactococcus lactis gene yjgB encodes a γ-d-glutaminyl-l-lysyl-endopeptidase which hydrolyzes petidoglycan. Appl Environ Microbiol 73 (in press).
    [Google Scholar]
  35. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  36. Shockman, G. D. ( 1992; ). The autolytic (‘suicidase’) system of Enterococcus hirae: from lysine depletion autolysis to biochemical and molecular studies of the two muramidases of Enterococcus hirae ATCC 9790. FEMS Microbiol Lett 79, 261–267.
    [Google Scholar]
  37. Shockman, G. D. & Höltje, J. V. ( 1994; ). Microbial peptidoglycan (murein) hydrolases. In Bacterial Cell Wall (New Comprehensive Biochemistry), vol. 27, pp. 131–167. Edited by J.-M. Ghuysen & R. Hackenbeck. Amsterdam, The Netherlands: Elsevier.
  38. Smith, T. J., Blackman, S. A. & Foster, S. J. ( 2000; ). Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146, 249–262.
    [Google Scholar]
  39. Steen, A., Buist, G., Leenhouts, K. J., El Khattabi, M., Grijpstra, F., Zomer, A. L., Venema, G., Kuipers, O. P. & Kok, J. ( 2003; ). Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J Biol Chem 278, 23874–23881.[CrossRef]
    [Google Scholar]
  40. Steen, A., Buist, G., Horsburgh, G. J., Venema, G., Kuipers, O. P., Foster, S. J. & Kok, J. ( 2005a; ). AcmA of Lactococcus lactis is an N-acetylglucosaminidase with an optimal number of LysM domains for proper functioning. FEBS J 272, 2854–2868.[CrossRef]
    [Google Scholar]
  41. Steen, A., Palumbo, E., Deghorain, M., Cocconcelli, P. S., Delcour, J., Kuipers, O. P., Kok, J., Buist, G. & Hols, P. ( 2005b; ). Autolysis of Lactococcus lactis is increased upon d-alanine depletion of peptidoglycan and lipoteichoic acids. J Bacteriol 187, 114–124.[CrossRef]
    [Google Scholar]
  42. Studier, F. W. & Moffatt, B. A. ( 1986; ). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113–130.[CrossRef]
    [Google Scholar]
  43. Towbin, H., Staehelin, T. & Gordon, J. ( 1979; ). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76, 4350–4354.[CrossRef]
    [Google Scholar]
  44. Vollmer, W. & Tomasz, A. ( 2000; ). The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J Biol Chem 275, 20496–20501.[CrossRef]
    [Google Scholar]
  45. Wecke, J., Madela, K. & Fischer, W. ( 1997; ). The absence of d-alanine from lipoteichoic acid and wall teichoic acid alters surface charge, enhances autolysis and increases susceptibility to methicillin in Bacillus subtilis. Microbiology 143, 2953–2960.[CrossRef]
    [Google Scholar]
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