Random mutagenesis identifies novel genes involved in the secretion of antimicrobial, cell wall-lytic enzymes by Lactococcus lactis

Applied and Environmental Microbiology

Volumn 74, Issue 24, 2008, Pages 7490-7496

  Yu, Pei Tan ^a   Giffard, Philip M ^c   Barry, Daniel G ^a   Huston, Wilhelmina M ^a   Turner, Mark S ^b  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; GENES; MUTAGENESIS; PROTEINS;

ANTI-MICROBIAL; CELL WALLS; CONTROL STRAINS; EXPRESSION CASSETTES; FOOD INDUSTRIES; GENE PRODUCTS; LACTIS STRAINS; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; LYSOSTAPHIN; LYTIC ENZYMES; PEPTIDOGLYCAN; RANDOM MUTAGENESISES; RECOMBINANT PROTEINS; TRANSMEMBRANE PROTEINS; TRANSPOSON MUTAGENESISES; UBIQUINONE;

ENZYME ACTIVITY;

LYSOSTAPHIN; PEPTIDOGLYCAN; UBIQUINONE;

ANTIMICROBIAL ACTIVITY; BACTERIOPHAGE; BACTERIUM; CATALYSIS; ENZYME ACTIVITY; FOOD INDUSTRY; GENE EXPRESSION; MUTATION; PHENOTYPE; PROTEIN; SECRETION;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM MUTANT; ENZYME RELEASE; GENE INSERTION; LACTOCOCCUS LACTIS; MUTAGENESIS; NONHUMAN;

BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA TRANSPOSABLE ELEMENTS; GENE ORDER; LACTOCOCCUS LACTIS; LYSOSTAPHIN; MUTAGENESIS, INSERTIONAL;

LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; POSIBACTERIA;

EID: 57449116983     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00767-08     Document Type: Article

References (42)

1. Budin-Verneuil, A., V. Pichereau, Y. Auffray, D. Ehrlich, and E. Maguin. 2007. Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7:2038-2046.
2. Cortes-Perez, N. G., I. Poquet, M. Oliveira, J. J. Gratadoux, S. M. Madsen, A. Miyoshi, G. Corthier, V. Azevedo, P. Langella, and L. G. Bermúdez-Humarán. 2006. Construction and characterization of a Lactococcus lactis strain deficient in intracellular ClpP and extracellular HtrA proteases. Microbiology 152:2611-2618.
3. Dajcs, J. J., E. B. Hume, J. M. Moreau, A. R. Caballero, B. M. Cannon, and R. J. O'Callaghan. 2000. Lysostaphin treatment of methicillin-resistant Staphylococcus aureus keratitis in the rabbit. Investig. Ophthalmol. Vis. Sci. 41:1432-1437.
4. Dajcs, J. J., B. A. Thibodeaux, E. B. Hume, X. Zheng, G. D. Sloop, and R. J. O'Callaghan. 2001 Lysostaphin is effective in treating methicillin-resistant Staphylococcus aureus endophthalmitis in the rabbit. Curr. Eye Res. 22:451-457.
5. Dieye, Y., S. Usai, F. Clier, A. Gruss, and J. C. Piard. 2001. Design of a protein-targeting system for lactic acid bacteria. J. Bacteriol. 183:4157-4166.
6. Du, W., J. R. Brown, D. R. Sylvester, J. Huang, A. F. Chalker, C. Y. So, D. J. Holmes, D. J. Payne, and N. G. Wallis. 2000. Two active forms of UDP-N-acetylglucosamine enolpyruvyl transferase in gram-positive bacteria. J. Bacteriol. 182:4146-4152.
7. Dupont, K., T. Janzen, F. K. Vogensen, J. Josephsen, and B. Stuer-Lauridsen. 2004. Identification of Lactococcus lactis genes required for bacteriophage adsorption. Appl. Environ. Microbiol. 70:5825-5832.
8. Duwat, P., S. D. Ehrlich, and A. Gruss. 1999. Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol. Microbiol. 31:845-858.
9. Ermolaeva, M. D., O. White, and S. L. Salzberg. 2001. Prediction of operons in microbial genomes. Nucleic Acids Res. 29:1216-1221.
10. Gasson, M. J. 1983. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 154:1-9.
11. Green, J. M., W. K. Merkel, and B. P. Nichols. 1992. Characterization and sequence of Escherichia coli pabC, the gene encoding aminodeoxychorismate lyase, a pyridoxal phosphate-containing enzyme. J. Bacteriol. 174:5317-5323.
12. Guillot, A., C. Gitton, P. Anglade, and M. Y. Mistou. 2003. Proteomic analysis of Lactococcus lactis, a lactic acid bacterium. Proteomics 3:337-354.
13. Frees, D., P. Varmanen, and H. Ingmer. 2001. Inactivation of a gene that is highly conserved in gram-positive bacteria stimulates degradation of nonnative proteins and concomitantly increases stress tolerance in Lactococcus lactis. Mol. Microbiol. 41:93-103.
14. Hirokawa, T., S. Boon-Chieng, and S. Mitaku. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379.
15. Hofmann, K., and W. Stoffel. 1993. TMbase - a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374:166.
16. Kock, H., U. Gerth, and M. Hecker. 2004. MurAA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp-dependent proteolysis in Bacillus subtilis. Mol. Microbiol. 51:1087-1102.
17. Kokai-Kun, J. F., T. Chanturiya, and J. J. Mond. 2007. Lysostaphin as a treatment for systemic Staphylococcus aureus infection in a mouse model. J. Antimicrob. Chemother. 60:1051-1059.
18. Loessner, M. J., G. Wendlinger, and S. Scherer. 1995. Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol. Microbiol. 16:1231-1241.
19. Maguin, E., H. Prévost, S. D. Ehrlich, and A. Gruss. 1996. Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J. Bacteriol. 178:931-935.
20. Marquardt, J. L., D. A. Siegele, R. Kolter, and C. T. Walsh. 1992. Cloning and sequencing of Escherichia coli murZ and purification of its product, a UDP-N-acetylglucosamine enolpyruvyl transferase. J. Bacteriol. 174:5748-5752.
21. Mierau, I., P. Leij, I. van Swam, B. Blommestein, E. Floris, J. Mond, and E. J. Smid. 2005. Industrial-scale production and purification of a heterologous protein in Lactococcus lactis using the nisin-controlled gene expression system NICE: the case of lysostaphin. Microb. Cell Fact. 4:15.
22. Mierau, I., K. Olieman, J. Mond, and E. J. Smid. 2005. Optimization of the Lactococcus lactis nisin-controlled gene expression NICE for industrial applications. Microb. Cell Fact. 4:16.
23. Miyoshi, A., I. Poquet, V. Azevedo, J. Commissaire, L. Bermúdez-Humarán, E. Domakova, Y. Le Loir, S. C. Oliveira, A. Gruss, and P. Langella. 2002. Controlled production of stable heterologous proteins in Lactococcus lactis. Appl. Environ. Microbiol. 68:3141-3146.
24. Nakano, S., E. Küster-Schöck, A. D. Grossman, and P. Zuber. 2003. Spxdependent transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 100:13603-13608.
25. Nouaille, S., J. Commissaire, J. J. Gratadoux, P. Ravn, A. Bolotin, A. Gruss, Y. Le Loir, and P. Langella. 2004. Influence of lipoteichoic acid D-alanylation on protein secretion in Lactococcus lactis as revealed by random mutagenesis. Appl. Environ. Microbiol. 70:1600-1607.
26. Nouaille, S., E. Morello, N. Cortez-Peres, Y. Le Loir, J. Commissaire, J. J. Gratadoux, E. Poumerol, A. Gruss, and P. Langella. 2006. Complementation of the Lactococcus lactis secretion machinery with Bacillus subtilis SecDF improves secretion of staphylococcal nuclease. Appl. Environ. Microbiol. 72:2272-2279.
27. Oluola, O., L. Kong, M. Fein, and L. E. Weisman. 2007. Lysostaphin in treatment of neonatal Staphylococcus aureus infection. Antimicrob. Agents Chemother. 51:2198-2200.
28. Patron, R. L., M. W. Climo, B. P. Goldstein, and G. L. Archer. 1999. Lysostaphin treatment of experimental aortic valve endocarditis caused by a Staphylococcus aureus isolate with reduced susceptibility to vancomycin. Antimicrob. Agents Chemother. 43:1754-1755.
29. Poquet, I., V. Saint, E. Seznec, N. Simoes, A. Bolotin, and A. Gruss. 2000. HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol. Microbiol. 35:1042-1051.
30. Price, M. N., K. H. Huang, E. J. Alm, and A. P. Arkin. 2005. A novel method for accurate operon predictions in all sequenced prokaryotes. Nucleic Acids Res. 33:880-892.
31. Ravn, P., J. Arnau, S. M. Madsen, A. Vrang, and H. Israelsen. 2003. Optimization of signal peptide SP310 for heterologous protein production in Lactococcus lactis. Microbiology 149:2193-2201.
32. Recsei, P. A., A. D. Gruss, and R. P. Novick. 1987. Cloning, sequence, and expression of the lysostaphin gene from Staphylococcus simulans. Proc. Natl. Acad. Sci. USA 84:1127-1131.
33. Rost, B., R. Casadio, P. Fariselli, and C. Sander. 1995. Transmembrane helices predicted at 95% accuracy. Protein Sci. 4:521-533.
34. Schindler, C. A., and V. T. Schuhardt. 1964. Lysostaphin: a new bacteriolytic agent for the Staphylococcus. Proc. Natl. Acad. Sci. USA 51:414-421.
35. Slock, J., D. P. Stahly, C. Y. Han, E. W. Six, and I. P. Crawford. 1990. An apparent Bacillus subtilis folic acid biosynthesis operon containing pab, an amphibolic trpG gene, a third gene required for synthesis of para-aminobenzoic acid, and the dihydropteroate synthase gene. J. Bacteriol. 172:7211-7226.
36. Stroobant, P., I. G. Young, and F. Gibson. 1972. Mutants of Escherichia coli K-12 blocked in the final reaction of ubiquinone biosynthesis: characterization and genetic analysis. J. Bacteriol. 109:134-139.
37. Turner, M. S., L. M. Hafner, T. Walsh, and P. M. Giffard. 2003. Peptide surface display and secretion using two LPXTG-containing surface proteins from Lactobacillus fermentum BR11. Appl. Environ. Microbiol. 69:5855-5863.
38. Turner, M. S., Y. P. Tan, and P. M. Giffard. 2007. Inactivation of an iron transporter in Lactococcus lactis results in resistance to tellurite and oxidative stress. Appl. Environ. Microbiol. 73:6144-6149.
39. Turner, M. S., F. Waldherr, M. J. Loessner, and P. M. Giffard. 2007. Antimicrobial activity of lysostaphin and a Listeria monocytogenes bacteriophage endolysin produced and secreted by lactic acid bacteria. Syst. Appl. Microbiol. 30:58-67.
40. Veiga, P., C. Bulbarela-Sampieri, S. Furlan, A. Maisons, M. P. Chapot-Chartier, M. Erkelenz, P. Mervelet, P. Noirot, D. Frees, O. P. Kuipers, J. Kok, A. Gruss, G. Buist, and S. Kulakauskas. 2007. SpxB regulates Oacetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J. Biol. Chem. 282:19342-19354.
41. Wegkamp, A., W. van Oorschot, W. M. de Vos, and E. J. Smid. 2007. Characterization of the role of para-aminobenzoic acid biosynthesis in folate production by Lactococcus lactis. Appl. Environ. Microbiol. 73:2673-2681.
42. Wegmann, U., M. O'Connell-Motherway, A. Zomer, G. Buist, C. Shearman, C. Canchaya, M. Ventura, A. Goesmann, M. J. Gasson, O. P. Kuipers, D. van Sinderen, and J. Kok. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189:3256-3270.