Probiotic bacteria survive in Cheddar cheese and modify populations of other lactic acid bacteria

Journal of Applied Microbiology

Volumn 116, Issue 6, 2014, Pages 1642-1656

  Ganesan, B ^a   Weimer, B C ^b   Pinzon, J ^b   Dao Kong, N ^b   Rompato, G ^a   Brothersen, C ^a   Mcmahon, D J ^a  

^a UTAH STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cheddar cheese; Low fat; Nonculturability; Probiotic; Survival

Indexed keywords

BACILLI; LACTIC ACID; POLYMERASE CHAIN REACTION;

BACTERIAL POPULATION; BACTERIAL SPECIES; CHEDDAR CHEESE; LACTIC ACID BACTERIA; LOW FAT; NONCULTURABILITY; PROBIOTIC BACTERIA; PROBIOTIC LACTOBACILLI; PROBIOTICS; SURVIVAL;

STARTERS;

LACTIC ACID; PROPIDIUM IODIDE;

COMPETITION (ECOLOGY); FOOD PROCESSING; FOOD QUALITY; GROWTH RATE; MICROBIAL ACTIVITY; POPULATION GROWTH; PROBIOTICS; SPECIES DIVERSITY; SURVIVORSHIP;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERIUM DETECTION; BIFIDOBACTERIUM ANIMALIS; CHEESE; CHEESEMAKING; CONTROLLED STUDY; FAT CONTENT; LACTIC ACID BACTERIUM; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS PARACASEI; LACTOCOCCUS LACTIS; NONHUMAN;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS PARACASEI; LACTOCOCCUS;

CHEDDAR CHEESE; LOW FAT; NONCULTURABILITY; PROBIOTIC; SURVIVAL;

ANIMALS; BIFIDOBACTERIUM; CHEESE; COLONY COUNT, MICROBIAL; LACTIC ACID; LACTOBACILLUS; MICROBIAL VIABILITY; MILK; POLYMERASE CHAIN REACTION; PROBIOTICS;

EID: 84900829784     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12482     Document Type: Article

References (84)

1. Achilleos, C. and Berthier, F. (2013) Quantitative PCR for the specific quantification of Lactococcus lactis and Lactobacillus paracasei and its interest for Lactococcus lactis in cheese samples. Food Microbiol 36, 286-295.
2. Auty, M.A., Gardiner, G.E., McBrearty, S.J., O'Sullivan, E.O., Mulvihill, D.M., Collins, J.K., Fitzgerald, G.F., Stanton, C. et al. (2001) Direct in situ viability assessment of bacteria in probiotic dairy products using viability staining in conjunction with confocal scanning laser microscopy. Appl Environ Microbiol 67, 420-425.
3. Banks, J. (2007) Producing low fat cheeses. In Improving the flavour of cheese ed. Weimer, B.C. pp. 520- 536. Cambridge, UK: Woodhead/CRC Press.
4. Baruzzi, F., Matarante, A., Caputo, L. and Morea, M. (2005) Development of a culture-independent polymerase chain reaction-based assay for the detection of lactobacilli in stretched cheese. J Rapid Methods Autom Microbiol 13, 177-192.
5. Beresford, T.P., Fitzsimons, N.A., Brennan, N.L. and Cogan, T.M. (2001) Recent advances in cheese microbiology. Int Dairy J 11, 259-274.
6. Bertoni, G., Calamari, L. and Maianti, M.G. (2001) Producing specific milks for speciality cheeses. Proc Nutr Soc 60, 231-246.
7. Branen, A.L. and Keenan, T.W. (1969) Growth stimulation of Lactobacillus species by lactic streptococci. Appl Microbiol 17, 280-285.
8. Buist, G., Karsens, H., Nauta, A., van Sinderen, D., Venema, G. and Kok, J. (1997) Autolysis of Lactococcus lactis caused by induced overproduction of its major autolysin, AcmA. Appl Environ Microbiol 63, 2722-2728.
9. Buist, G., Venema, G. and Kok, J. (1998) Autolysis of Lactococcus lactis is influenced by proteolysis. J Bacteriol 180, 5947-5953.
10. Byun, R., Nadkarni, M.A., Chhour, K.L., Martin, F.E., Jacques, N.A. and Hunter, N. (2004) Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 42, 3128-3136.
11. Caglar, E., Kargul, B. and Tanboga, I. (2005) Bacteriotherapy and probiotics' role on oral health. Oral Dis 11, 131-137.
12. Chou, L.-S. (2001) The arginine deiminase pathway in lactococci: physiological role and molecular characterization. Nutrition and Food Sciences. Logan: Utah State University.
13. Chou, L.-S., Weimer, B.C. and Cutler, R. (2001) Relationship of arginine and lactose utilization by Lactococcus lactis ssp. lactis ML3. Int Dairy J 11, 253-258.
14. Coolbear, T., Wilkinson, M.G. and Weimer, B.C. (2011) Lactic acid bacteria: LAB in flavour development. In Encyclopedia of Dairy Science ed. Fuquay, J.F., Fox, P.F. and McSweeney, P.L. pp. 160-165. London, UK: Elsevier/Academic Press.
15. Crow, V.L., Coolbear, T., Holland, R., Pritchard, G.G. and Marttley, F.G. (1993) Starters as finishers: starter properties relevant to Cheese ripening. Int Dairy J 3, 423-460.
16. Crow, V.L., Coolbear, T., Gopal, P.K., Martley, F.G., McKay, L.L. and Riepe, H. (1995) The role of autolysis of lactic acid bacteria in the ripening of cheese. Int Dairy J 5, 855-875.
17. Crow, V., Curry, B. and Hayes, M. (2001) The ecology of non-starter lactic acid bacteria (NSLAB) and their use as adjuncts in New Zealand Cheddar. Int Dairy J 11, 275-283.
18. Daigle, A., Roy, D., Belanger, G. and Vuillemard, J.C. (1999) Production of probiotic cheese (cheddar-like cheese) using enriched cream fermented by Bifidobacterium infantis. J Dairy Sci 82, 1081-1091.
19. Dasen, A., Berthier, F., Grappin, R., Williams, A.G. and Banks, J. (2003) Genotypic and phenotypic characterization of the dynamics of the lactic acid bacterial population of adjunct-containing Cheddar cheese manufactured from raw and microfiltered pasteurised milk. J Appl Microbiol 94, 595-607.
20. Delroisse, J.-M., Boulvin, A.-L., Parmentier, I., Dauphin, R.D., Vandenbol, M. and Portetelle, D. (2008) Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiol Res 163, 663-670.
21. Dinakar, P. and Mistry, V.V. (1994) Growth and viability of Bifidobacterium bifidum in cheddar cheese. J Dairy Sci 77, 2854-2864.
22. FAO/WHO. (2002) Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. Guidelines for the evaluation of probiotics in food: report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. London, ON, Canada.
23. Fasoli, S., Marzotto, M., Rizzotti, L., Rossi, F., Dellaglio, F. and Torriani, S. (2003) Bacterial composition of commercial probiotic products as evaluated by PCR-DGGE analysis. Int J Food Microbiol 82, 59-70.
24. Fenelon, M.A., O'Connor, P. and Guinee, T.P. (2000) The effect of fat content on the microbiology and proteolysis in cheddar cheese during ripening dairy foods. J Dairy Sci 83, 2173-2183.
25. Fernandez, M., del Rio, B., Linares, D.M., Martin, M.C. and Alvarez, M.A. (2006) Real-time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J Dairy Sci 89, 3763-3769.
26. Fitzsimons, N.A., Cogan, T.M., Condon, S. and Beresford, T. (2001) Spatial and temporal distribution of non-starter lactic acid bacteria in Cheddar cheese. J Appl Microbiol 90, 600-608.
27. Fox, P.F. and Wallace, J.M. (1997) Formation of flavour compounds in cheese. Adv Appl Microbiol 45, 17-85.
28. Fukushima, H., Katsube, K., Hata, Y., Kishi, R. and Fujiwara, S. (2007) Rapid separation and concentration of food-borne pathogens in food samples prior to quantification by viable-cell counting and real-time PCR. Appl Environ Microbiol 73, 92-100.
29. Ganesan, B., Seefeldt, K. and Weimer, B.C. (2004) Fatty acid production from amino acids and α-keto acids by Brevibacterium linens BL2. Appl Environ Microbiol 70, 6385-6393.
30. Ganesan, B., Dobrowolski, P. and Weimer, B.C. (2006) Identification of the catabolic pathway of leucine-to-2-methylbutyric acid by Lactococcus lactis. Appl Environ Microbiol 72, 4264-4273.
31. Ganesan, B., Stuart, M.R. and Weimer, B.C. (2007) Carbohydrate starvation causes a metabolically active but nonculturable state in Lactococcus lactis. Appl Environ Microbiol 73, 2498-2512.
32. Garcia-Cayuela, T., Tabasco, R., Pelaez, C. and Requena, T. (2009) Simultaneous detection and enumeration of viable lactic acid bacteria and bifidobacteria in fermented milk by using propidium monoazide and real-time PCR. Int Dairy J 19, 405-409.
33. Gardiner, G., Ross, R.P., Collins, J.K., Fitzgerald, G. and Stanton, C. (1998) Development of a probiotic cheddar cheese containing human-derived Lactobacillus paracasei strains. Appl Environ Microbiol 64, 2192-2199.
34. Gardiner, G.E., Ross, R.P., Wallace, J.M., Scanlan, F.P., Jagers, P.P., Fitzgerald, G.F., Collins, J.K. and Stanton, C. (1999a) Influence of a probiotic adjunct culture of Enterococcus faecium on the quality of cheddar cheese. J Agric Food Chem 47, 4907-4916.
35. Gardiner, G., Stanton, C., Lynch, P.B., Collins, J.K., Fitzgerald, G. and Ross, R.P. (1999b) Evaluation of cheddar cheese as a food carrier for delivery of a probiotic strain to the gastrointestinal tract. J Dairy Sci 82, 1379-1387.
36. Garrigues, C., Johansen, E. and Pedersen, M.B. (2010) Complete genome sequence of Bifidobacterium animalis subsp. lactis BB-12, a widely consumed probiotic strain. J Bacteriol 192, 2467-2468.
37. Giraffa, G. and Rossetti, L. (2004) Monitoring of the bacterial composition of dairy starter cultures by RAPD-PCR. FEMS Microbiol Lett 237, 133-138.
38. Gomez-Donate, M., Balleste, E., Muniesa, M. and Blanch, A.R. (2012) New molecular quantitative PCR assay for detection of host-specific Bifidobacteriaceae suitable for microbial source tracking. Appl Environ Microbiol 78, 5788-5795.
39. van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S.D. and Maguin, E. (2002) Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82, 187-216.
40. Habibi-Najafi, M.B. and Lee, B.H. (1996) Bitterness in cheese: a review. Crit Rev Food Sci Nutr 36, 397-411.
41. Heller, K.J. (2001) Probiotic bacteria in fermented foods: product characteristics and starter organisms. Am J Clin Nutr 73, 374S-379S.
42. Henri-Dubernet, S., Desmasures, N. and Gueguen, M. (2008) Diversity and dynamics of lactobacilli populations during ripening of RDO Camembert cheese. Can J Microbiol 54, 218-228.
43. Ibrahim, F., Ruvio, S., Granlund, L., Salminen, S., Viitanen, M. and Ouwehand, A.C. (2010) Probiotics and immunosenescence: cheese as a carrier. FEMS Immunol Med Microbiol 59, 53-59.
44. Kailasapathy, K. (2002) Microencapsulation of probiotic bacteria: technology and potential applications. Curr Issues Intest Microbiol 3, 39-48.
45. Kilcawley, K.N., Nongonierma, A.B., Hannon, J.A., Doolan, I.A. and Wilkinson, M.G. (2011) Evaluation of commercial enzyme systems to accelerate Cheddar cheese ripening. Int Dairy J 26, 50-57.
46. Klein, G., Pack, A., Bonaparte, C. and Reuter, G. (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41, 103-125.
47. Klijn, N., Weerkamp, A.H. and de Vos, W.M. (1995) Detection and characterization of lactose-utilizing Lactococcus spp. in natural ecosystems. Appl Environ Microbiol 61, 788-792.
48. Kramer, M., Obermajer, N., Bogovic Matijasic, B., Rogelj, I. and Kmetec, V. (2009) Quantification of live and dead probiotic bacteria in lyophilised product by real-time PCR and by flow cytometry. Appl Microbiol Biotechnol 84, 1137-1147.
49. Macfarlane, G.T., Steed, H. and Macfarlane, S. (2008) Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J Appl Microbiol 104, 305-344.
50. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N. et al. (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103, 15611-15616.
51. Matsuki, T., Watanabe, K., Fujimoto, J., Kado, Y., Takada, T., Matsumoto, K. and Tanaka, R. (2004) Quantitative PCR with 16S rRNA-gene-targeted species-specific primers for analysis of human intestinal bifidobacteria. Appl Environ Microbiol 70, 167-173.
52. Mc Brearty, S., Ross, R.P., Fitzgerald, G.F., Collins, J.K., Wallace, J.M. and Stanton, C. (2001) Influence of two commercially available bifidobacteria cultures on Cheddar cheese quality. Int Dairy J 11, 599-610.
53. McSweeney, P.L.H., Fox, P.F., Lucey, J.A., Jordan, K.N. and Cogan, T.M. (1993) Contribution of the indigenous microflora to the maturation of Cheddar cheese. Int Dairy J 3, 613-634.
54. Medici, M., Vinderola, C.G. and Perdigon, G. (2004) Gut mucosal immunomodulation by probiotic fresh cheese. Int Dairy J 14, 611-618.
55. Mengheri, E. (2008) Health, probiotics, and inflammation. J Clin Gastroenterol 42(Suppl 3, Pt 2), S177-S178.
56. Midje, D.L., Bastian, E.D., Morris, H.A., Martin, F.B., Bridgeman, T. and Vickers, Z.M. (2000) Flavor enhancement of reduced fat cheddar cheese using an integrated culturing system. J Agric Food Chem 48, 1630-1636.
57. Monnet, C., Correia, K., Sarthou, A.S. and Irlinger, F. (2006) Quantitative detection of Corynebacterium casei in cheese by real-time PCR. Appl Environ Microbiol 72, 6972-6979.
58. Monnet, C., Ulve, V., Sarthou, A.S. and Irlinger, F. (2008) Extraction of RNA from cheese without prior separation of microbial cells. Appl Environ Microbiol 74, 5724-5730.
59. Morelli, L. and Capurso, L. (2012) FAO/WHO guidelines on probiotics: 10 years later. J Clin Gastroenterol 46, S1-S2.
60. Moreno Villares, J.M. (2008) Probiotics in infant formulae. Could we modify the immune response? An Pediatr (Barc) 68, 286-294.
61. Nocker, A., Sossa-Fernandez, P., Burr, M.D. and Camper, A.K. (2007) Use of propidium monoazide for live/dead distinction in microbial ecology. Appl Environ Microbiol 73, 5111-5117.
62. Oberg, C.J., Moyes, L.V., Domek, M.J., Brothersen, C. and McMahon, D.J. (2011) Survival of probiotic adjunct cultures in cheese and challenges in their enumeration using selective media. J Dairy Sci 94, 2220-2230.
63. Ogier, J.C., Son, O., Gruss, A., Tailliez, P. and Delacroix-Buchet, A. (2002) Identification of the bacterial microflora in dairy products by temporal temperature gradient gel electrophoresis. Appl Environ Microbiol 68, 3691-3701.
64. Ong, L. and Shah, N.P. (2008) Influence of probiotic Lactobacillus acidophilus and L. helveticus on proteolysis, organic acid profiles, and ACE-inhibitory activity of cheddar cheeses ripened at 4, 8, and 12 degrees C. J Food Sci 73, M111-M120.
65. O'Sullivan, D., Ross, R.P., Fitzgerald, G.F. and Coffey, A. (2000) Investigation of the relationship between lysogeny and lysis of Lactococcus lactis in cheese using prophage-targeted PCR. Appl Environ Microbiol 66, 2192-2198.
66. Ouwehand, A.C., Ibrahim, F. and Forssten, S.D. (2012) Cheese as a carrier for probiotics: in vitro and human studies. Aust J Dairy Technol 65, 165-169.
67. Peterson, S.D. and Marshall, R.T. (1990) Nonstarter lactobacilli in cheddar cheese: a review. J Dairy Sci 73, 1395-1410.
68. Phillips, M., Kailasapathy, K. and Tran, L. (2006) Viability of commercial probiotic cultures (L. acidophilus, Bifidobacterium sp., L. casei, L. paracasei and L. rhamnosus) in cheddar cheese. Int J Food Microbiol 108, 276-280.
69. Rademaker, J.L.W., Hoolwerf, J.D., Wagendorp, A.A. and te Giffel, M.C. (2006) Assessment of microbial population dynamics during yoghurt and hard cheese fermentation and ripening by DNA population fingerprinting. Int Dairy J 16, 457-466.
70. Rallu, F., Gruss, A. and Maguin, E. (1996) Lactococcus lactis and stress. Antonie Van Leeuwenhoek 70, 243-251.
71. Rantsiou, K., Alessandria, V., Urso, R., Dolci, P. and Cocolin, L. (2008) Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR. Int J Food Microbiol 121, 99-105.
72. Rossetti, L. and Giraffa, G. (2005) Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. J Microbiol Methods 63, 135-144.
73. Rudi, K., Naterstad, K., Dromtorp, S.M. and Holo, H. (2005) Detection of viable and dead Listeria monocytogenes on gouda-like cheeses by real-time PCR. Lett Appl Microbiol 40, 301-306.
74. Salama, M., Sandine, W. and Giovannoni, S. (1991) Development and application of oligonucleotide probes for identification of Lactococcus lactis subsp. cremoris. Appl Environ Microbiol 57, 1313-1318.
75. Sharp, M.D., McMahon, D.J. and Broadbent, J.R. (2008) Comparative evaluation of yogurt and low-fat cheddar cheese as delivery media for probiotic Lactobacillus casei. J Food Sci 73, M375-M377.
76. Sheu, S.J., Hwang, W.Z., Chen, H.C., Chiang, Y.C. and Tsen, H.Y. (2009) Development and use of tuf gene-based primers for the multiplex PCR detection of Lactobacillus acidophilus, Lactobacillus casei group, Lactobacillus delbrueckii, and Bifidobacterium longum in commercial dairy products. J Food Prot 72, 93-100.
77. Sieuwerts, S., de Bok, F.A., Hugenholtz, J. and van Hylckama Vlieg, J.E. (2008) Unraveling microbial interactions in food fermentations: from classical to genomics approaches. Appl Environ Microbiol 74, 4997-5007.
78. Sohier, D., Jamet, E., Le Dizes, A.S., Dizin, M., Pavan, S., Postollec, F. and Coton, E. (2012) Polyphasic approach for quantitative analysis of obligately heterofermentative Lactobacillus species in cheese. Food Microbiol 31, 271-277.
79. Swearingen, P.A., O'Sullivan, D.J. and Warthesen, J.J. (2001) Isolation, characterization, and influence of native, nonstarter lactic acid bacteria on Cheddar cheese quality. J Dairy Sci 84, 50-59.
80. Trepanier, G., Simard, R.E. and Lee, B.H. (1991) Effect of added lactobacilli on composition and texture of Cheddar cheese during accelerated maturation. J Food Sci 56, 696-700.
81. Vasquez, A., Ahrne, S., Pettersson, B. and Molin, G. (2001) Temporal temperature gradient gel electrophoresis (TTGE) as a tool for identification of Lactobacillus casei, Lactobacillus paracasei, Lactobacillus zeae and Lactobacillus rhamnosus. Lett Appl Microbiol 32, 215-219.
82. Ventura, M., Reniero, R. and Zink, R. (2001) Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach. Appl Environ Microbiol 67, 2760-2765.
83. de Vrese, M. and Schrezenmeir, J. (2008) Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111, 1-66.
84. Yu, Z., Dong, B. and Lu, W. (2009) Dynamics of bacterial community in solid-state fermented feed revealed by 16S rRNA. Lett Appl Microbiol 49, 166-172.