1887

Abstract

A gene encoding a putative peptidoglycan hydrolase, named , which is a paralogue of the major autolysin gene, was identified in the genome sequence. The gene is transcribed in MG1363 and its expression is modulated during cellular growth. The encoded AcmB protein has a modular structure with three domains: an N-terminal domain, especially rich in Ser, Thr, Pro and Asn residues, resembling a cell-wall-associated domain; a central domain homologous to the muramidase catalytic domain; and a C-terminal domain of unknown function. A recombinant AcmB derivative, devoid of its N-terminal domain, was expressed in . It exhibited hydrolysing activity on the peptidoglycan of several Gram-positive bacteria, including . Though showing sequence similarity with enterococcal muramidase, AcmB has acetylglucosaminidase specificity. The gene was inactivated in order to evaluate the role of the enzyme. AcmB does not appear to be involved in cell separation but contributes to cellular autolysis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25875-0
2003-03-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/3/mic149695.html?itemId=/content/journal/micro/10.1099/mic.0.25875-0&mimeType=html&fmt=ahah

References

  1. Anba J, Bidnenko E, Hillier A, Ehrlich D., Chopin M. C. 1995; Characterization of the lactococcal abiD1 gene coding for phage abortive infection. J Bacteriol 177:3818–3823
    [Google Scholar]
  2. 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]
  3. Baba T., Schneewind O. 1998; Targeting of muralytic enzymes to the cell division site of Gram-positive bacteria: repeat domains direct autolysin to the equatorial surface ring of Staphylococcus aureus . EMBO J 17:4639–4646
    [Google Scholar]
  4. Bateman A., Bycroft M. 2000; The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD. J Mol Biol 299:1113–1119
    [Google Scholar]
  5. Biswas I, Gruss A, Ehrlich S. D., Maguin E. 1993; High-efficiency gene inactivation and replacement system for gram-positive bacteria. J Bacteriol 175:3628–3635
    [Google Scholar]
  6. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich S. D., Sorokin A. 2001; The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11:731–753
    [Google Scholar]
  7. Bolotin A, Ehrlich S. D., Sorokin A. 2002; Studies of genomes of dairy bacteria Lactococcus lactis . Sci Aliment 22:45–53
    [Google Scholar]
  8. Buist G. 1997 AcmA of Lactococcus lactis, a cell-binding major autolysin PhD thesis University of Groningen; Netherlands:
    [Google Scholar]
  9. 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]
  10. Buist G, Karsens H, Nauta A, van Sinderen D, Venema G., Kok J. 1997; Autolysis of Lactococcus lactis caused by induced overproduction of its major autolysin, AcmA. Appl Environ Microbiol 63:2722–2728
    [Google Scholar]
  11. 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
    [Google Scholar]
  12. Chapot-Chartier M. P. 1996; Les autolysines des bactéries lactiques. Lait 76:91–109
    [Google Scholar]
  13. Chapot-Chartier M. P, Deniel C, Rousseau M., Gripon J. C. 1994; Autolysis of two strains of Lactococcus lactis during cheese ripening. Int Dairy J 4:251–269
    [Google Scholar]
  14. 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
    [Google Scholar]
  15. 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
    [Google Scholar]
  16. Chu C. P, Kariyama R, Daneo-Moore L., Shockman G. D. 1992; Cloning and sequence analysis of the muramidase-2 gene from Enterococcus hirae . J Bacteriol 174:1619–1625
    [Google Scholar]
  17. Cibik R, Lepage E., Talliez P. 2000; Molecular diversity of Leuconostoc mesenteroides and Leuconostoc citreum isolated from traditional French cheeses as revealed by RAPD fingerprinting, 16S rDNA sequencing and 16S rDNA fragment amplification. Syst Appl Microbiol 23:267–278
    [Google Scholar]
  18. Cibik R, Talliez P, Langella P., Chapot-Chartier M. P. 2001; Identification of Mur, an atypical peptidoglycan hydrolase derived from Leuconostoc citreum . Appl Environ Microbiol 67:858–864
    [Google Scholar]
  19. Crow V. L, Coolbear T, Gopal F. G, Martley F. G, McKay L. L., Riepe H. 1995; The role of autolysis of lactic acid bacteria in the ripening of cheese. Int Dairy J 5:855–875
    [Google Scholar]
  20. Drouault S, Corthier G, Ehrlich S. D., Renault P. 1999; Survival, physiology, and lysis of Lactococcus lactis in the digestive tract. Appl Environ Microbiol 65:4881–4886
    [Google Scholar]
  21. Fischetti V. A, Pancholi V., Schneewind O. 1990; Conservation of a hexapeptide sequence in the anchor region of surface proteins from Gram-positive cocci. Mol Microbiol 4:1603–1605
    [Google Scholar]
  22. Fischetti V. A, Pancholi V., Schneewind O. 1991; Common characteristics of the surface proteins from gram-positive cocci. In Genetics and Molecular Biology of Streptococci, Lactococci and Enterococci pp  290–294 Edited by Dunny G. M., Cleary P. P., McKay L. L. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Gasson M. J. 1983; Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 154:1–9
    [Google Scholar]
  24. Gibson T. J. 1984 Studies on the Epstein-Barr genome PhD thesis University of Cambridge; UK:
    [Google Scholar]
  25. Holo H., Nes I. F. 1995; Transformation of Lactococcus by electroporation. Methods Mol Biol 47:195–199
    [Google Scholar]
  26. Horsburgh G. J. 2001 The role of autolysins of Bacillus subtilis 168 during cell growth and differentiation PhD thesis University of; Sheffield, UK:
    [Google Scholar]
  27. Husson-Kao C, Mengaud J, Benbadis L., Chapot-Chartier M. P. 2000; Mur1, a Streptococcus thermophilus peptidoglycan hydrolase devoid of a specific cell wall binding domain. FEMS Microbiol Lett 187:69–76
    [Google Scholar]
  28. Joris B, Englebert S, Chu C. P, Kariyama R, Daneo-Moore L, Shockman G. D., Ghuysen J. M. 1992; Modular design of the Enterococcus hirae muramidase-2 and Streptococcus faecalis autolysin. FEMS Microbiol Lett 70:257–264
    [Google Scholar]
  29. 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]
  30. Kuroda M, Ohta T, Uchiyama I. 34 other authors 2001; Whole genome sequencing of methicillin-resistant Staphylococcus aureus . Lancet 357:1225–1240
    [Google Scholar]
  31. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  32. Lepeuple A. S, Van Gemert E., Chapot-Chartier M. P. 1998; Analysis of the bacteriolytic enzymes of the autolytic Lactococcus lactis subsp. cremoris strain AM2 by renaturing polyacrylamide gel electrophoresis: identification of a prophage-encoded enzyme. Appl Environ Microbiol 64:4142–4148
    [Google Scholar]
  33. Mainardi J. L, Legrand R, Arthur M, Schoot B, van Heijenoort J., Gutmann L. 2000; Novel mechanism of beta-lactam resistance due to bypass of dd-transpeptidation in Enterococcus faecium . J Biol Chem 275:16490–16496
    [Google Scholar]
  34. McIver K. S, Subbarao S, Kellner E. M, Heath A. S., Scott J. R. 1996; Identification of isp , a locus encoding an immunogenic secreted protein conserved among group A streptococci. Infect Immun 64:2548–2555
    [Google Scholar]
  35. Moens S., Vanderleyden J. 1997; Glycoproteins in prokaryotes. Arch Microbiol 168:169–175
    [Google Scholar]
  36. Morton T. M, Eaton D. M, Johnston J. L., Archer G. L. 1993; DNA sequence and units of transcription of the conjugative transfer gene complex (trs) of Staphylococcus aureus plasmid pGO1. J Bacteriol 175:4436–4447
    [Google Scholar]
  37. Nielsen H, Engelbrecht J, Brunak S., von Heijne G. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6
    [Google Scholar]
  38. Niven G. W., Mulholland F. 1998; Cell membrane integrity and lysis in Lactococcus lactis : the detection of a population of permeable cells in post-logarithmic phase cultures. J Appl Microbiol 84:90–96
    [Google Scholar]
  39. Pillidge C. J, Govindasamy-Lucey S, Gopal P. K., Crow V. L. 1998; The major lactococcal cell wall autolysin AcmA does not determine the rate of autolysis of Lactococcus lactis subsp. cremoris 2250 in cheddar cheese. Int Dairy J 8:843–850
    [Google Scholar]
  40. Pospiech A., Neumann B. 1995; A versatile quick-prep of genomic DNA from gram-positive bacteria. Trends Genet 11:217–218
    [Google Scholar]
  41. Ramadurai L, Lockwood K. J, Nadakavukaren M. J., Jayaswal R. K. 1999; Characterization of a chromosomally encoded glycylglycine endopeptidase of Staphylococcus aureus . Microbiology 145:801–808
    [Google Scholar]
  42. Rathsam C., Jacques N. A. 1998; Role of C-terminal domains in surface attachment of the fructosyltransferase of Streptococcus salivarius ATCC 25975. J Bacteriol 180:6400–6403
    [Google Scholar]
  43. Rathsam C, Giffard P. M., Jacques N. A. 1993; The cell-bound fructosyltransferase of Streptococcus salivarius : the carboxyl terminus specifies attachment in a Streptococcus gordonii model system. J Bacteriol 175:4520–4527
    [Google Scholar]
  44. Sambrook J, Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  45. Shockman G. D., Höltje J. V. 1994; Microbial peptidoglycan (murein) hydrolases. In New Comprehensive Biochemistry, vol. 27, Bacterial Cell Wall pp 131–167 Edited by Guysen J.-M., Hakenbeck R. Amsterdam: Elsevier Science;
    [Google Scholar]
  46. 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]
  47. Steen A, Buist G, Horsburgh G, Foster S, Kuipers O., Kok J. 2001; AcmA is a glucosaminidase. In Abstracts, Eurolab Conference, 3–6 July 2001 Cork, Irish Republic. :
    [Google Scholar]
  48. Trieu-Cuot P, de Cespedes G., Horaud T. 1992; Nucleotide sequence of the chloramphenicol resistance determinant of the streptococcal plasmid pIP501. Plasmid 28:272–276
    [Google Scholar]
  49. Tusnady G. E., Simon I. 2001; The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850
    [Google Scholar]
  50. van Asseldonk M, Rutten G, Oteman M, Siezen R. J, de Vos W. M., Simons G. 1990; Cloning of usp45 , a gene encoding a secreted protein from Lactococcus lactis subsp. lactis MG1363. Gene 95:155–160
    [Google Scholar]
  51. Walker S. A., Klaenhammer T. R. 2001; Leaky Lactococcus cultures that externalize enzymes and antigens independently of culture lysis and secretion and export pathways. Appl Environ Microbiol 67:251–259
    [Google Scholar]
  52. Wells J. M, Robinson K, Chamberlain L. M, Schofield K. M., Le Page R. W. 1996; Lactic acid bacteria as vaccine delivery vehicles. Antonie Van Leeuwenhoek 70:317–330
    [Google Scholar]
  53. Wilkinson G. M, Guinee T. P, O'Callaghan D. M., Fox P. F. 1994; Autolysis and proteolysis in different strains of starter bacteria during cheddar cheese ripening. J Dairy Res 61:249–262
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25875-0
Loading
/content/journal/micro/10.1099/mic.0.25875-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error