Development of bacteriocinogenic strains of Saccharomyces cerevisiae heterologously expressing and secreting the leaderless enterocin L50 peptides L50A and L50B from Enterococcus faecium L50

Applied and Environmental Microbiology

Volumn 75, Issue 8, 2009, Pages 2382-2392

  Basanta, Antonio ^a   Herranz, Carmen ^a   Gutiérrez, Jorge ^a   Criado, Raquel ^a   Hernández, Pablo E ^a   Cintas, Luis M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-MICROBIAL PEPTIDES; ENTEROCIN; ENTEROCOCCUS FAECIUM; EXPRESSION VECTORS; S. CEREVISIAE; SACCHAROMYCES CEREVISIAE; STABLE EXPRESSIONS; STRUCTURAL GENES;

CLONING; GENE ENCODING; PEPTIDES;

AMINES;

ENTEROCIN L50A; ENTEROCIN L50B; MATING HORMONE ALPHA FACTOR; MATING HORMONE ALPHA FACTOR 1; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

CLONE; GENE EXPRESSION; PEPTIDE; SECRETION; YEAST;

ARTICLE; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; EXPRESSION VECTOR; MOLECULAR CLONING; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SECRETION; SACCHAROMYCES CEREVISIAE; STRUCTURAL GENE;

ANTI-INFECTIVE AGENTS; BACTERIOCINS; ENTEROCOCCUS FAECIUM; MASS SPECTROMETRY; MICROBIAL SENSITIVITY TESTS; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN SORTING SIGNALS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE;

ENTEROCOCCUS FAECIUM; SACCHAROMYCES CEREVISIAE;

EID: 64749101378     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01476-08     Document Type: Article

References (49)

1. Basanta, A., J. Sánchez, B. Gómez-Sala, C. Herranz, P. E. Hernández, and L. M. Cintas. 2008. Antimicrobial activity of Enterococcus faecium L50, a strain producing enterocins L50 (L50A and L50B), P and Q, against beer spoilage lactic acid bacteria in broth, wort (hopped and unhopped), and alcoholic and non-alcoholic lager beers. Int. J. Food Microbiol. 125:293-307.
2. Beaulieu, L., D. Groleau, C. B. Miguez, J. F. Jetté, H. Aomari, and M. Subirade. 2005. Production of pediocin PA-1 in the methylotrophic yeast P. pastoris reveals unexpected inhibition of its biological activity due to the presence of collagen-like material. Protein Expr. Purif. 43:111-125.
3. Bhunia, A. K., M. G. Johnson, and B. Ray. 1987. Direct detection of an antimicrobial peptide of Pediococcus acidilactici in sodium dodecyl sulphatepolyacrylamide gel electrophoresis. J. Ind. Microbiol. 2:319-322.
4. Brot, N., and H. Weissbach. 1991. Biochemistry of methionine sulfoxide residues in proteins. Biofactors 3:91-96.
5. Casaus, M. P., T. Nilsen, L. M. Cintas, I. F. Nes, and P. E. Hernández. 1997. Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology 143:2287-2294.
6. Cereghino, J. L., and J. M. Cregg. 2000. Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol. Rev. 24:45-66.
7. Cintas, L. M., J. M. Rodríguez, M. F. Fernández, K. Sletten, I. F. Nes, P. E. Hernández, and H. Holo. 1995. Isolation and characterization of pediocin L50, a new bacteriocin from Pediococcus acidilactici with a broad inhibitory spectrum. Appl. Environ. Microbiol. 61:2643-2648.
8. Cintas, L. M., P. Casaus, H. Holo, P. E. Hernández, I. F. Nes, and L. S. Håvarstein. 1998. Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins. J. Bacteriol. 180:1988-1994.
9. Cintas, L. M., P. Casaus, M. F. Fernández, and P. E. Hernández. 1998. Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A and lactocin S against spoilage and foodborne pathogenic bacteria. Food Microbiol. 15:289-298.
10. Cintas, L. M., P. Casaus, C. Herranz, L. S. Håvarstein, H. Holo, P. E. Hernández, and I. F. Nes. 2000. Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, the sec- dependent enterocin P, and a novel bacteriocin secreted without an N- terminal extension termed enterocin Q. J. Bacteriol. 182:6806- 6814.
11. Cintas, L. M., P. Casaus, C. Herranz, I. F. Nes, and P. E. Hernández. 2001. Bacteriocins of lactic acid bacteria. Food Sci. Technol. Int. 7:281-305.
12. Cleveland, J., T. J. Montville, I. F. Nes, and M. L. Chikindas. 2001. Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1-20.
13. Cotter, P. D., C. Hill, and R. P. Ross. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788.
14. Criado, R., J. Gutiérrez, M. Martín, C. Herranz, P. E. Hernández, and L. M. Cintas. 2006. Immunochemical characterization of temperature-regulated production of enterocin L50 (EntL50A and EntL50B), enterocin P, and enterocin Q by Enterococcus faecium L50. Appl. Environ. Microbiol. 72: 7634-7643.
15. Deegan, L. H., P. D. Cotter, C. Hill, and P. Ross. 2006. Bacteriocins: biological tools for bio-preservation and shelf-life extension. Int. Dairy J. 16: 1058-1071.
16. Delves-Broughton, J., P. Blackburn, R. J. Evans, and J. Hugenholtz. 1996. Applications of the bacteriocin, nisin. Antonie van Leeuwenhoek 69:193-202.
17. Drider, D., G. Fimland, Y. Héchard, L. M. McMullen, and H. Prévost. 2006. The continuing story of class IIa bacteriocins. Microbiol. Mol. Biol. Rev. 70:564-582.
18. Fimland, G., V. G. H. Eijsink, and J. Nissen-Meyer. 2002. Comparative studies of immunity proteins of pediocin-like bacteriocins. Microbiology 148:3661-3670.
19. Franz, C. M. A. P., M. J. van Belkum, W. H. Holzapfel, H. Abriouel, and A. Gálvez. 2007. Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol. Rev. 31:293-310.
20. Gajic, O., G. Buist, M. Kojic, L. Topisirovic, O. P. Kuipers, and J. Kok. 2003. Novel mechanism of bacteriocin secretion and immunity carried out by lactococcal multidrug resistance proteins. J. Biol. Chem. 278:34291-34298.
21. Garneau, S., N. I. Martin, and J. C. Vederas. 2002. Two-peptide bacteriocins produced by lactic acid bacteria. Biochimie 84:577-592.
22. Gutiérrez, J., R. Criado, R. Citti, M. Martín, C. Herranz, M. F. Fernández, L. M. Cintas, and P. E. Hernández. 2004. Performance and applications of polyclonal antipeptide antibodies specific for the enterococcal bacteriocin enterocin P. J. Agric. Food Chem. 52:2247-2255.
23. Gutiérrez, J., D. Bourque, R. Criado, Y. J. Choi, L. M. Cintas, P. E. Hernández, and C. B. Míguez. 2005. Heterologous extracellular production of enterocin P from Enterococcus faecium P13 in the methylotrophic bacterium Methylobacterium extorquens. FEMS Microbiol. Lett. 248:125-131.
24. Hammond, J. R. 1995. Genetically-modified brewing yeasts for the 21st century. Progress to date. Yeast 11:1613-1627.
25. Holo, H., Ø. Nilssen, and I. F. Nes. 1991. Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene. J. Bacteriol. 173:3879-3887.
26. Ilgen, C., J. L. Cereghino, and J. M. Cregg. 2005. Pichia pastoris, p. 143-162. In G. Gellissen (ed.), Production of recombinant proteins: novel microbial and eucaryotic expression systems. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
27. Izquierdo, E., A. Bednarczyk, C. Schaeffer, Y. Cai, E. Marchioni, A. van Dorsselaer, and S. Ennahar. 2008. Production of enterocins L50A, L50B, and IT, a new enterocin, by Enterococcus faecium IT62, a strain isolated from Italian ryegrass in Japan. Antimicrob. Agents Chemother. 52:1917-1923.
28. Jespersen, L. 2003. Occurrence and taxonomic characteristics of strains of Saccharomyces cerevisiae predominant in African indigenous fermented foods and beverages. FEMS Yeast Res. 3:191-200.
29. Johnsen, L., G. Fimland, V. Eijsink, and J. Nissen-Meyer. 2000. Engineering increased stability in the antimicrobial peptide pediocin PA-1. Appl. Environ. Microbiol. 66:4798-4802.
30. Johnsen, L., G. Fimland, and J. Nissen-Meyer. 2005. The C-terminal domain of pediocin-like antimicrobial peptides (class IIa bacteriocins) is involved in specific recognition of the C-terminal part of cognate immunity proteins and in determining the antimicrobial spectrum. J. Biol. Chem. 280:9243-9250.
31. Kazazic, M., J. Nissen-Meyer, and G. Fimland. 2002. Mutational analysis of the role of charged residues in target-cell binding, potency and specificity of the pediocin-like bacteriocin sakacin P. Microbiology 148:2019-2027.
32. Kieleczawa, J. 2006. Fundamentals of sequencing of difficult templates - an overview. J. Biomol. Tech. 17:207-217.
33. Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-85.
34. Line, J. E., E. A. Svetoch, B. V. Eruslanov, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. P. Levchuk, O. E. Svetoch, B. S. Seal, G. R. Siragusa, and N. J. Stern. 2008. Isolation and purification of enterocin E-760 with broad antimicrobial activity against gram-positive and gram-negative bacteria. Antimicrob. Agents Chemother. 52:1094-1100.
35. Linko, M., A. Haikara, A. Ritala, and M. Penttilä. 1998. Recent advances in the malting and brewing industry. J. Biotechnol. 65:85-98.
36. Nes, I. F., D. B. Diep, L. S. Håvarstein, M. B. Brurberg, V. Eijsink, and H. Holo. 1996. Biosynthesis of bacteriocins in lactic acid bacteria. Antonie van Leeuwenhoek 70:113-128.
37. Nes, I. F., D. B. Diep, and H. Holo. 2007. Bacteriocin diversity in Streptococcus and Enterococcus. J. Bacteriol. 189:1189-1198.
38. Oliveira, C. C., J. J. van den Heuvel, and J. E. McCarthy. 1993. Inhibition of translational initiation in Saccharomyces cerevisiae by secondary structure: the roles of the stability and position of stem-loops in the mRNA leader. Mol. Microbiol. 9:521-532.
39. Ross, R. P., S. Morgan, and C. Hill. 2002. Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79:3-16.
40. Sakamoto, K., and W. N. Konings. 2003. Beer spoilage bacteria and hop resistance. Int. J. Food Microbiol. 89:105-124.
41. Sánchez-Hidalgo, M., M. Maqueda, A. Gálvez, H. Abriouel, E. Valdivia, and M. Martínez-Bueno. 2003. The genes coding for enterocin EJ97 production by Enterococcus faecalis EJ97 are located on a conjugative plasmid. Appl. Environ. Microbiol. 69:1633-1641.
42. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
43. Schiffer, M., C.-H. Chang, and F. J. Stevens. 1992. The function of tryptophan residues in membrane proteins. Protein Eng. 5:213-214.
44. Schoeman, H., M. A. Vivier, M. du Toit, L. M. T. Dicks, and I. S. Pretorius. 1999. The development of bactericidal yeast strains by expressing the Pediococcus acidilactici pediocin gene (pedA)in Saccharomyces cerevisiae. Yeast 15:647-656.
45. Schuster, M., A. Einhauer, E. Wasserbauer, F. Süßenbacher, C. Ortner, M. Paumann, G. Werner, and A. Jungbauer. 2000. Protein expression in yeast; comparison of two expression strategies regarding protein maturation. J. Biotechnol. 84:237-248.
46. Van Reenen, C. A., M. L. Chikindas, W. H. van Zyl, and L. M. T. Dicks. 2003. Characterization and heterologous expression of a class IIa bacteriocin, plantaricin 423 from Lactobacillus plantarum 423, in Saccharomyces cerevisiae. Int. J. Food Microbiol. 81:29-40.
47. Vaughan, A., T. O'Sullivan, and D. van Sinderen. 2005. Enhancing the microbiological stability of malt and beer - a review. J. Inst. Brew. 111:355-371.
48. Vega Laso, M. R., D. Zhu, F. Sagliocco, A. J. Brown, M. F. Tuite, and J. E. McCarthy. 1993. Inhibition of translational initiation in the yeast Saccharomyces cerevisiae as a function of the stability and position of hairpin structures in the mRNA leader. J. Biol. Chem. 268:6453-6462.
49. Weissbach, H., F. Etienne, T. Hoshi, S. H. Heinemann, W. T. Lowther, B. Matthews, G. St John, C. Nathan, and N. Brot. 2002. Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch. Biochem. Biophys. 397:172-178.