Technological properties and probiotic potential of Enterococcus faecium strains isolated from cow milk

Journal of Applied Microbiology

Volumn 114, Issue 1, 2013, Pages 229-241

  Banwo, K ^a,b   Sanni, A ^a   Tan, H ^b  

^a UNIVERSITY OF IBADAN   (Nigeria)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Enterocin A; Enterococcus faecium; Milk; Nono; Safety

Indexed keywords

BACILLI; BACILLUS CEREUS; BODY FLUIDS; FERMENTATION; FERMENTED MILK; FOOD PROCESSING; LACTIC ACID; SALTS;

BACTERIOCINS; ENTEROCIN; ENTEROCIN A; ENTEROCOCCUS FAECIUM; MILK; NONO; PROBIOTICS; SAFETY INVESTIGATION; STARTER CULTURES; TECHNOLOGICAL PROPERTIES;

BACTERIOLOGY;

AMYLASE; BACTERIOCIN; BILE SALT; CATALASE; COLLAGEN TYPE 4; FIBRINOGEN; FIBRONECTIN; PEPSIN A; PROBIOTIC AGENT; TRIACYLGLYCEROL LIPASE;

ANTIBIOTICS; BACTERIUM; FERMENTATION; GENOTYPE; MILK; PHENOTYPE; PROBIOTICS;

ACIDIFICATION; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC SENSITIVITY; ARTICLE; BACILLUS CEREUS; BACILLUS SUBTILIS; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; CANDIDA ALBICANS; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; ENZYME ACTIVITY; ESCHERICHIA COLI O157; GENOTYPE; HEAT; HEMOLYSIS; HYDROLYSIS; IN VITRO STUDY; LACTOBACILLUS CASEI; LACTOBACILLUS FERMENTUM; LACTOBACILLUS PENTOSUS; LACTOBACILLUS PLANTARUM; LISTERIA MONOCYTOGENES; MICROCOCCUS LUTEUS; MILK; NONHUMAN; PEDIOCOCCUS ACIDILACTICI; PEDIOCOCCUS PENTOSACEUS; PH; PHENOTYPE; SAFETY; STAPHYLOCOCCUS AUREUS;

BACILLUS CEREUS; BACILLUS SUBTILIS; ENTEROCOCCUS FAECIUM; LISTERIA MONOCYTOGENES; MICROCOCCUS LUTEUS;

EID: 84871160996     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12031     Document Type: Article

References (61)

1. Al-Jabouri, M.M. and Al-Meshhadani, N.S. (1985) A note on antibiotic-resistant Escherichia coli in adult man, raw sewage and sewage polluted River Tigris in Mosul (Iraq). J Appl Bacteriol 59, 513-518.
2. Andrighetto, C., Knijff, E., Lombardi, A., Torriani, S., Vancanneyt, M., Kersters, K., Swings, J. and Dellaglio, F. (2001) Phenotypic and genetic diversity of enterococci isolated from Italian Cheeses. J Dairy Res 68, 303-316.
3. Banwo, K., Sanni, A.I., Tan, H.R. and Tian, Y.Q. (2012) Phenotypic and genotypic characterization of lactic acid bacteria isolated from some Nigerian traditional fermented foods. Food Biotechnol, 26(2), 124-142.
4. Ben-Omar, N., Castro, A., Lucas, R., Abriouel, H., Yousif, N.M.K., Franz, C.M.A.P., Holzapfel, W.H., Pérez-Pulido, R. et al. (2004) Functional and safety aspects of enterococci isolated from different Spanish foods. Syst Appl Microbiol 27, 118-130.
5. Brosius, J., Palmer, M.L., Kennedy, P.J. and Noller, H.F. (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sc USA 75, 4801-4805.
6. Callewaert, R., Holo, H., Devreese, B., Van Beeumen, J., Nes, I. and De Vuyst, L. (1999) Characterization and production of amylovorin L471, a bacteriocin purified from Lactobacillus amylovorus DCE 471 by a novel three-step method. Microbiol 145, 2559-2568.
7. Cocolin, L., Foschino, R., Comi, G.M. and Fortina, G. (2007) Description of the bacteriocins produced by two strains of Enterococcus faecium isolated from Italian goat milk. Food Microbiol 24, 752-758.
8. De Vuyst, L., Foulquie Moreno, M.R. and Revets, H. (2003) Screening for enterocins and detection of hemolysin and vancomycin resistance in enterococci of different origins. Int J Food Microbiol 84, 299-318.
9. Du Toit, M., Franz, C.M.A.P., Dicks, L.M.T. and Holzapfel, W.H. (2000) Preliminary characterization of bacteriocins produced by Enterococcus faecium and Enterococcus faecalis isolated from pig faeces. J Appl Microbiol, 88, 482-494.
10. Eaton, T.J. and Gasson, M.J. (2001) Molecular screening of enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol, 67, 1628-1635.
11. Eka, O.U. and Ohaba, J.A. (1977) Microbiological examination of Fulani milk (nono) and butter (man shanu). Nig J Sci, 11, 113-122.
12. Ennahar, S., Sashihara, T., Sonomoto, K. and Isahizaki, A. (2001) Class IIa bacteriocins; biosynthesis, structure and activity. FEMS Microbiol Rev 24, 85-106.
13. Foulquie-Moreno, M.R., Rea, M.C., Cogan, T.M. and De Vuyst, L. (2003) Applicability of a bacteriocin-producing Enterococcus faecium as co-culture in Cheddar cheese manufacture. Int J Food Microbiol 81, 73-84.
14. Franz, C.M.A.P., Schillinger, U. and Holzapfel, W.H. (1996) Production and characterization of enterocin 900, a bacteriocin produced by Enterococcus faecium BFE 900 from black olives. Int J Food Microbiol 29, 255-270.
15. Franz, C.M.A.P., Worobo, R.W., Quadri, L.E.N., Schillinger, U., Holzapfel, W.H., Vedras, J.C. and Stiles, M.E. (1999) Atypical genetic locus associated with constitutive production of enterotoxin B by Enterococcus faecium BFE 900. Appl Environ Microbiol 65, 2170-2178.
16. Franz, C.M.A.P., Muscholl-Silberhorn, A.B., Yousif, N.M.K., Vancanneyt, M., Swings, J. and Holzapfel, W.H. (2001) Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 6, 4385-4389.
17. Fuller, R. (1989) A review: probiotics in man and animals. J Appl Bacteriol 66, 365-378.
18. Giraffa, G. (2003) Functionality of enterococci in dairy products. Int J Food Microbiol 88, 215-222.
19. Hummel, A.S., Holzapfel, W.H. and Franz, C.M.A.P. (2007) Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst Appl Microbiol 30, 1-7.
20. Javed, I., Ali, M.I., Ahmed, B., Ghumro, P.B., Abdul, H. and Safia, A. (2011) Optimization and partial purification of bacteriocins from Enterococcus spp indigenous to Pakistan. Food Biotechnol 25, 130-139.
21. Johnston, L.M. and Jaykus, L. (2004) Antimicrobial resistance to Enterococcus species isolated from produce. Appl Environ Microbiol, 70, 3133-3137.
22. Kapczynski, D.R., Meinersmann, R.J. and Lee, M.D. (2000) Adherence of Lactobacillus to intestinal 407 cells in culture correlates with fibronectin binding. Curr Microbiol 41, 136-141.
23. Kayser, F.H. (2003) Safety aspects of enterococci from the medical point of view. Int J Food Microbiol, 88, 255-262.
24. Klaenhammer, T.R. (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12, 39-86.
25. Knorr, D. (1998) Technological aspects related to microorganisms in functional foods. Trends Food Sc Technol 9, 295-306.
26. Kostinek, M., Specht, I., Edward, V.A., Schillinger, U., Hertel, C., Holzapfel, W.H. and Franz, C.M.A.P. (2005) Diversity and technological properties of predominant lactic acid bacteria from fermented cassava used for the preparation of Gari, a traditional African food. Syst Appl Microbiol 28, 527-540.
27. Kostinek, M., Specht, I., Edward, V.A., Pinto, C., Egounlety, M., Sossa, C., Mbugua, S., Dorti, C. et al. (2007) Characterization and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int J Food Microbiol, 114, 342-351.
28. Kostrzynska, M., Paulsson, M., Schmidt, K.H. and Wadstrom, T. (1992) Comparative studies on binding of vitronectin and fibronectin to groups A and C streptococci. Microbios 71, 179-192.
29. Leroy, F. and De Vuyst, L. (2003) A combined model to predict the functionality of the bacteriocin-producing Lactobacillus sakei strain CTC494. Appl Environ Microbiol 69, 1093-1099.
30. Liong, M.T. and Shah, N.P. (2005) Acid, bile tolerance and cholesterol removal ability of lactobacilli strains. J Dairy Sc 88, 55-66.
31. Lopes, M.F.S., Ribeiro, T., Martins, M.P., Tenreiro, R. and Crespo, M.T.B. (2003) Gentamicin resistance in dairy and clinical Enterococcal isolates and in reference strains. J Ant Chem 52, 214-219.
32. Lorca, G., Torino, M.I., Font de Valdez, G. and Ljungh, A. (2002) Lactobacilli express cell surface proteins which mediate binding of immobilized collagen and Fibronectin. FEMS Microbiol Lett 206, 31-37.
33. Mannu, L., Paba, A., Daga, E., Comunian, R., Zanetti, S., Dupre, I. and Sechi, L.A. (2003) Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. Int J Food Microbiol, 88, 291-304.
34. Mathara, J.M., Schillinger, U., Kutima, P.M., Mbugua, S.K., Guigas, C., Franz, C. and Holzapfel, W.H. (2008) Functional properties of Lactobacillus plantarum strains isolated from Maasai Traditional Fermented Milk Products in Kenya. Curr Microbiol 56, 315-321.
35. Mathur, S. and Singh, R. (2005) Antibiotic resistance in food lactic acid bacteria - a review. Int J Food Microbiol 105, 281-295.
36. Minelli, E.B., Benini, A., Marzotto, M., Sbarbati, A., Ruzzenente, O., Ferrario, R. and Hendriks, H. (2004) Assessment of novel probiotic Lactobacillus casei strains for the production of functional dairy foods. Int Dairy J, 14, 723-736.
37. Morandi, S., Brasca, M., Andrighetto, C., Lombardi, A. and Lodi, R. (2006) Technological and molecular characterization of enterococci isolated from north-west Italian dairy products. Int Dairy J, 16, 867-875.
38. Morelli, L. (2000) In vitro selection of probiotic Lactobacilli: a critical appraisal. Curr Issues Intestinal Microbiol 1(2), 59-67.
39. Mueller, J.H. and Hinton, J. (1941) A protein-free medium for primary isolation of the Gonococcus and Meningococcus. Proc Soc Exp Biol Med 48, 330-333.
40. National Committee for Clinical Laboratory Standards (1990) Methods of Antimicrobial Susceptibility Testing of Anaerobic Bacteria, 2nd edn. Approved standard MII-AZ. Philadelphia, PA, Villanova, USA: National Committee for Clinical Laboratory Standards.
41. Oguntoyinbo, F.A. (2007) Identification and functional properties of dominant lactic acid bacteria isolated at different stages of solid state fermentation of cassava during Gari production. W J Microbiol Biotechnol, 23, 1425-1432.
42. Olasupo, N.A., Schillinger, U., Narbad, A., Dodd, H. and Holzapfel, W.H. (1999) Occurrence of nisin Z production in Lactococcus lactis BFE 1500 isolated from wara, a traditional Nigerian cheese product. Int J Food Microbiol 53, 141-152.
43. Parente, E. and Ricciardi, A. (1999) Production, recovery and purification of bacteriocins from lactic acid bacteria. Appl Microbiol Biotechnol 52, 628-638.
44. Park, S.H., Itoh, K. and Fujisawa, T. (2003) Characteristics and identification of enterocins produced by Enterococcus faecium JCM 5804. J Appl Microbiol, 95, 294-300.
45. Prasad, S., Morris, P., Hansen, R., Meaden, P.G. and Austin, B. (2005) A novel bacteriocin-like substance (BLIS) from a pathogenic strain of Vibrio harveyi. Microbiol 151, 3051-3058.
46. Rodriguez, E., Gonzalez, B., Gaya, P., Nunez, M. and Medina, M. (2000) Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J 10, 7-15.
47. Sambrook, J.E., Eritsch, F. and Maniatis, J. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold spring harbor, NY: Cold spring habour Laboratory Press.
48. Sarantinopoulous, P., Kalantzopoulous, G. and Tsakalõdou, E. (2001) Citrate metabolism by Enterococcus faecalis FAIR-E229. Appl Environ Microbiol 67, 5482-5487.
49. Schillinger, U. and Lucke, F.K. (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55, 1901-1906.
50. Schillinger, U., Guigas, C. and Holzapfel, W.H. (2005) In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 15, 1289-1297.
51. Strompfova, V. and Laukova, A. (2007) In vitro study on bacteriocin production of enterococci associated with chickens. Anaerobe, 13, 228-237.
52. Todorov, S.D. and Dicks, L.M.T. (2006) Screening for bacteriocin producing lactic acid bacteria from boza, a traditional cereal beverage from Bulgaria. Comparison of the bacteriocins. Proc Biochem 41, 11-19.
53. Villani, F. and Coppola, S. (1994) Selection of enterococcal strains for water-buffalo Mozzarella cheese manufacture. Ann Rev Microbial Enzymol 44, 97-105.
54. Vinderola, C.G. and Reinheimer, J.A. (2003) Lactic acid starter and probiotic bacteria, a comparative 'in vitro' study of probiotic characteristics and biological barrier resistance. Food Res Int 36, 895-904.
55. Vizoso-Pinto, M.G., Franz, C.M.A.P., Schillinger, U. and Holzapfel, W.H. (2006) Lactobacillus spp. with in vitro probiotic properties from human faeces and traditional fermented products. Int J Food Microbiol 109, 205-214.
56. Wadstrom, T., Andersson, K., Sydow, M., Axelsson, L., Lindgren, S. and Gullmar, B. (1987) Surface properties of lactobacilli isolated from the small intestine of pigs. J Appl Bacteriol 62, 513-520.
57. Walker, D.K. and Gilliland, S.E. (1993) Relationships among bile tolerance, bile salt deconjugation and assimilation of cholesterol by Lactobacillus acidophilus. J Dairy Sc 76, 956-961.
58. Yamamoto, Y., Togawa, Y., Shimosaka, M. and Okazaki, M. (2003) Purification and characterization of a novel bacteriocin produced by Enterococcus faecalis strain RJ-11. Appl Environ Microbiol 69, 5746-5753.
59. Yoon, M.Y., Kim, Y.J. and Hwang, H.J. (2008) Properties and safety aspects of Enterococcus faecium strains isolated from Chungkukjang, a fermented soy product. LWT, 41, 925-933.
60. Yousif, N.M.K., Dawyndt, P., Abriouel, H., Wijaya, A., Schillinger, U., Vancanneyt, M., Swings, J., Dirar, H.A. et al. (2005) Molecular characterization, technological properties and safety aspects of enterococci from 'Hussuwa', an African fermented sorghum product. J Appl Microbiol 98, 216-228.
61. Zareba, T.W., Pascu, C., Hryniewicz, W. and Wadstrom, T. (1997) Binding of extracellular matrix proteins by enterococci. Curr Microbiol 34, 6-11.