Characterization and antimicrobial spectrum of bacteriocins produced by lactic acid bacteria isolated from traditional Bulgarian dairy products

Journal of Applied Microbiology

Volumn 106, Issue 2, 2009, Pages 692-701

  Simova, E D ^a   Beshkova, D B ^a   Dimitrov, Zh P ^b  

^a INSTITUTE OF MICROBIOLOGY   (Bulgaria)

^b LB Bulgaricum Research and Development Centre   (Bulgaria)

Author keywords

Bacteriocin; Enterococcus; Inhibitory spectrum; Lactobacillus; Lactococcus

Indexed keywords

ANTIMICROBIAL AGENTS; BACILLI; LACTIC ACID;

ANTI-BACTERIAL ACTIVITY; ANTIMICROBIAL SPECTRA; BACTERIOCINS; ENTEROCOCCUS; INHIBITORY SPECTRUMS; LACTIC ACID BACTERIA; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOCOCCUS; WIDE SPECTRUM;

DAIRY PRODUCTS;

AMYLASE; BACTERIOCIN; BULGARICIN; PROTEINASE; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

AMINO ACID; ANIMAL PRODUCT; ANTIMICROBIAL ACTIVITY; BACTERIUM; ENZYME ACTIVITY; HOMOLOGY; ISOLATED POPULATION; MOLECULAR ANALYSIS; PEPTIDE;

AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; CONTROLLED STUDY; DAIRY PRODUCT; DRUG DETERMINATION; ENTEROCOCCUS FAECIUM; HEAT TOLERANCE; HIGH TEMPERATURE; LACTIC ACID BACTERIUM; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LACTOCOCCUS LACTIS; MOLECULAR WEIGHT; NONHUMAN; PH; PROTEIN ANALYSIS; STRUCTURAL HOMOLOGY;

ENTEROCOCCUS; ENTEROCOCCUS FAECIUM; HELICOBACTER PYLORI; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; LACTOBACILLUS PLANTARUM; LACTOCOCCUS; LACTOCOCCUS LACTIS;

EID: 58549084006     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2008.04052.x     Document Type: Article

References (58)

1. Aktypis, A., Kalantzopoulos, G., Huis In't Veld, J.H.J. Ten Brink, B. (1998) Purification and characterization of thermophilin T, a novel bacteriocin produced by Streptococcus thermophilus ACA-DC 0040. J Appl Microbiol 84, 568 576.
2. Barefoot, S.F. Klaenhammer, T.R. (1983) Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl Environ Microbiol 45, 1808 1815.
3. Bezkorovainy, A. (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73 (Suppl. s399 s405.
4. Cesena, C., Morelli, L., Alander, M., Siljander, T., Tuomola, E., Salminen, S., Mattila-Sandholm, T., Vilpponen-Salmela, T. et al. (2001) Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J Dairy Sci 84, 1001 1010.
5. Chen, Y., Shapira, R., Eisentein, M. Montville, T.J. (1997) Functional characterization of pediocin PA-1 binding to liposomes in the absence of a protein receptor and its relationship to a predicted tertiary structure. Appl Environ Microbiol 63, 524 531.
6. Collado, M.C., Hernández, M. Sanz, Y. (2005a) Production of bacteriocin-like compounds by human feacal Bifidobacterium strains. J Food Protect 68, 1034 1040.
7. Collado, M.C., Gonzaléz, A., Gonzaléz, R., Hernández, M., Ferrús, M.A. Sanz, Y. (2005b) Antimicrobial peptides are among the antagonistic metabolites produced by Bifidobacterium against Helicobacter pylori. Int J Antimicrob Agents 25, 385 391.
8. Corsetti, A., Settanni, L. Van Sinderen, D. (2004) Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. J Appl Microbiol 96, 521 534.
9. Danone Nutritopics 2002) Effect of Probiotics on Body's Natural Defenses. Special Issue, July 2002.
10. Danone Nutritopics 2004) The Health Benefits of Probiotics. N 29, March 2004.
11. De Camps, C., Maroncle, N., Balestrino, D., Rich, C. Forestier, C. (2003) Persistence of colonozation of intestinal mucosa by a probiotic strain, Lactobacillus casei subsp. rhamnosus Lcr35, after oral consumption. J Clin Microbiol 41, 1270 1273.
12. Dimitrov, Z., Michaylova, M. Minkova, S. (2005) Characterization of Lactobacillus helveticus strains isolated from Bulgarian yoghurt, cheese, plants and human faecal samples by sodium dodecylsulfate polycrylamide gel electrophoresis of cell-wall proteins, ribotyping and pulsed field gel fingerprinting. Int Dairy J 15, 998 1005.
13. Ducluzeau, R. (2001) Lactic acid bacteria viability or implantation in the digestive tract: two unmistakable features. Yoghurt Ferment Milk Lett 5, 1 5.
14. Eijsink, V.G.H., Skeie, M., Middelhoven, P.H., Brurberg, M.B. Nes, I.F. (1998) Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl Environ Microbiol 64, 3275 3281.
15. Eijsink, V.G.H., Axelsson, L., Diep, D.B., Havarstein, L.S., Holo, H. Nes, I.F. (2002) Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie von Leeuwenhoek 81, 639 654.
16. Elegado, F.B., Querra, M.A.R.V., Macayan, R.A., Mendoza, H.A. Lizaran, M.B. (2004) Spectrum of bacteriocin activity of Lactobacillus plantarum BS and fingerprinting by RAPD-PCR. Int J Food Microbiol 95, 11 18.
17. Ennahar, S., Sashihara, T., Sonomoto, K. Ishizaki, A. (2000) Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol Rev 24, 85 106.
18. Fimland, G., Johnsen, L., Axelsson, L., Brurberg, M.B., Nes, I.F., Eijsink, V.G.H. Nissen-Meyer, J. (2000) A C-terminal disulfide bridge in pediocin-like bacteriocins renders bacteriocin activity less temperature dependent and is a major determinant of antimicrobial spectrum. J Bacteriol 182, 2643 2648.
19. Flynn, S., Van Sinderen, D., Thornton, G.M., Holo, H., Nes, I.F. Collins, J.K. (2002) Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology 148, 973 984.
20. Forestier, C., De Camps, C., Vatoux, C. Joly, B. (2001) Probiotic activities of Lactobacillus casei subsp. rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res Microbiol 152, 167 173.
21. Gagnon, M., Kheadr, E.E., Le Blay, G. Fliss, I. (2004) In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin. Int J Food Microbiol 92, 69 78.
22. Giraffa, G., Gatti, M., Rossetti, L., Senini, L. Neviani, E. (2000) Molecular diversity within Lactobacillus helveticus as revealed by genotypic characterization. Appl Environ Microbiol 66, 1259 1265.
23. Guerra, N.P. Pastrana, L. (2002) Modelling the influence of pH on the kinetics of both nisin and pediocin production and characterization of their functional properties. Process Biochem 37, 1005 1015.
24. Hosono, A. (2001) Nutritional and Physiological Properties of Lactic Acid Bacteria. 64 pp. Japan : JICA.
25. Huang, H.W. (1999) Peptide-lipid interactions and mechanisms of antimicrobial peptides. Novart Found Symp 225, 188 200.
26. Hudault, S., Liévin, V., Bernet-Camard, M.F. Servin, A. (1997) Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (Strain GG) against Salmonella typhimurium C5 infection. Appl Environ Microbiol 63, 513 518.
27. IDF Standard 149 A 1997) Dairy Starter Cultures of Lactic Acid Bacteria (LAB) - Standard of Identity. Brussels, Belgium : International Dairy Federation.
28. IDF Standard 163 1992) General Standard of Identity for Fermented Milks. Brussels, Belgium : International Dairy Federation.
29. Juárez Tomás, M.S., Bru, E., Wiese, B., de Ruiz Holgado, A.A.P. Nader-Macías, M.E. (2002) Influence of pH, temperature and culture media on the growth and bacteriocin production by vaginal Lactobacillus salivarius CRL 1328. J Appl Microbiol 93, 714 724.
30. Kim, T.S., Hur, J.W., Yu, M.A., Cheigh, C.I., Kim, K.N., Hwang, J.K. Pyun, Y.R. (2003) Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J Food Protect 66, 3 12.
31. Klaenhammer, T.R. (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12, 39 86.
32. Kojima, S., Takizawa, S., Tamura, S., Fujinaga, S., Benno, Y. Nakase, T. (1993) An improved medium for the isolation of lactobacilli from kefir grains. Biosci Biotechnol Biochem 57, 119 120.
33. Lavermicocca, P., Valeria, F., Evidente, A., Lazzaroni, S., Corsetti, A. Gobbetti, M. (2000) Purification and characterization of novel antifungal compounds by sourdough Lactobacillus plantarum 21 B. Appl Environ Microbiol 66, 4084 4090.
34. Magnusson, J. Schnurer, J. (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Appl Environ Microbiol 67, 1 5.
35. Messens, W. De Vuyst, L. (2002) Inhibitory substances produced by Lactobacilli isolated from sourdoughs - a review. Int J Food Microbiol 72, 31 43.
36. Meydani, M. Ha, W. (2000) Immunologic effects of yoghurt. Am J Clin Nutr 71, 861 872.
37. Navarro, L., Zarazaga, M., Sáenz, J., Riuz-Larrea, F. Torres, C. (2000) Bacteriocin production by lactic acid bacteria isolated from Rioja red vines. J Appl Microbiol 88, 44 51.
38. Nes, I.F., Diep, D.B., Havarstein, L.S., Brurberg, M.B., Eijsink, V. Holo, H. (1996) Biosynthesis of bacteriocins in lactic acid bacteria. Antonie von Leeuwenhoek 70, 113 128.
39. Nes, I.F., Holo, H., Fimland, G., Hauge, H.H. Nissen-Meyer, J. (2002) Unmodified peptide-bacteriocins (class II) produced by lactic acid bacteria. In Peptide, Antibiotics, Discovery, Modes of Action and Application ed. Dutton, C.J., Haxell, M.A., McArthur, H.A.I. Wax, R.C. pp. 81 116 New York : Marcel Dekker.
40. Okkers, D.J., Disks, L.M.T., Silvester, M., Joubert, J.J. Odendaal, H.L. (1999) Characterization of pediocin TV35b, a bacteriocin-like peptide isolated from Lactobacillus pentosus with a fungistatic effect on Candida albicans. J Appl Microbiol 87, 726 734.
41. Parente, E. Ricciardi, A. (1999) Production, recovery and purification of bacteriocins from lactic acid bacteria. Appl Microbiol Biotechnol 52, 628 638.
42. Pernoud, S., Schneid-Citrain, N., Agnetti, V., Breton, S., Faurie, J.M., Marchal, L., Obis, D., Oudot, D. et al. (2005) Application des bacteries lactiques dans les produits laitiers frais et effets des probiotiques. In Bacteries Lactiques et Probiotiques ed. Luquet, F.M. Corrieu, G. pp. 1 106 France : Lavoisier.
43. Remiger, A., Eijsink, V.G.H., Ehrmann, M.A., Sletten, K., Nes, I.F. Vogel, R.F. (1999) Purification and partial amino acid sequence of plantaricin 1.25α and 1.25β, two bacteriocins produced by Lactobacillus plantarum TMW1.25. J Appl Microbiol 86, 1053 1058.
44. Rodriguez, J.M., Cintas, L.M., Casans, P., Suarez, A. Hernandez, P.E. (1995) PCR detection of the lactocin S structural gene in bacteriocin-producing lactobacilli from meat. Appl Environ Microbiol 61, 2802 2805.
45. Rodríguez, E., González, B., Gaya, P., Nùñez, M. Medina, M. (2000) Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J 10, 7 15.
46. Rodtong, S. Tannock, G.W. (1993) Differentiation of Lactobacillus strains by ribotyping. Appl Environ Microbiol 59, 3480 3484.
47. Seegers, J.F. (2002) Lactobacilli as live vaccine delivery vectors: progress and prospects. Trends Biotechnol 20, 508 515.
48. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236 248.
49. Simova, E., Beshkova, D., Angelov, A., Hristozova, T.S., Frengova, G. Spasov, Z. (2002) Lactic acid bacteria and yeasts in kefir grains and kefir made from them. J Ind Microbiol Biotechnol 28, 1 6.
50. Simova, E., Beshkova, D., Najdenski, H., Frengova, G., Simov, Z. Tsvetkova, I. (2006) Antimicrobial-producing lactic acid bacteria from traditional Bulgarian milk products: inhibitory properties and in situ bacteriocinogenic activity. In Proceedings of the IUFoST, 13th World Congress Food Sci Technol "Food is live", Nantes, France, Vol. 685, pp. 907 908.
51. Simova, E., Beshkova, D., Angelov, M. Dimitrov, Z.H. (2008) Bacteriocin production by strain Lactobacillus delbrueckii ssp. bulgaricus BB18 during continuous prefermentation of yogurt starter culture and subsequent batch coagulation of milk. J Ind Microbiol Biotechnol 35, 559 567.
52. Soomro, A.H., Masud, T. Anwaar, K. (2002) Role of lactic acid bacteria (LAB) in food preservation and human health - a review. Pakistan J Nutr 1, 20 24.
53. Sreekumar, O. Hosono, A. (2000) Immediate effect of Lactobacillus acidophilus on the intestinal flora and faecal enzymes of rats and the in vivo inhibition of Escherichia coli coculture. J Dairy Sci 83, 931 939.
54. Tannock, G.W. (2000) Molecular assessment of the intestinal microflora. Am J Clin Nutr 73, s401 s414.
55. Tichaczek, P.S., Nissen-Meyer, J., Nes, I.F., Vogel, R.F. Nammers, W.P. (1992) Characterization of the bacteriocins curvacin A from Lactobacillus curvatus LTH1174 and sakacin P from Lactobacillus sake LTH673. Syst Appl Microbiol 15, 460 468.
56. Van de Guchte, M., Ehrlich, S.D. Maguin, E. (2001) Production of growth-inhibiting factors by Lactobacillus delbrueckii. J Appl Microbiol 91, 147 153.
57. Van Reenen, C.A., Dicks, L.M. Chikindas, M.L. (1998) Isolation, purification and partial characterization of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum. J Appl Microbiol 84, 1131 1137.
58. Vaughan, A., Eijsink, V.G.H., O'Sullivan, T.F., O'Hanlon, K. Van Sinderen, D. (2001) An analysis of bacteriocins produced by lactic acid bacteria isolated from malted barley. J Appl Microbiol 91, 131 138.