Journal of Dairy Science
Volume 90, Issue 10 , Pages 4532-4542 , October 2007

Nonstarter Lactobacillus Strains as Adjunct Cultures for Cheese Making: In Vitro Characterization and Performance in Two Model Cheeses

Received 8 March 2007 ,Accepted 13 June 2007.

References 

  1. Banks JM, Williams AG. The role of the non-starter lactic acid bacteria in Cheddar cheese ripening. Int. J. Dairy Technol. 2004;57:145–152
  2. Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM. Recent advances in cheese microbiology. Int. Dairy J. 2001;11:259–274
  3. Bergamini CV, Hynes E, Zalazar CA. Proteolysis patterns in a probiotic semihard cheese. Int. Dairy J. 2006;16:856–866
  4. Binetti AG, Bailo NB, Reinheimer JA. Spontaneous phage-resistant mutants of Streptococcus thermophilus: Isolation and technological characteristics. Int. Dairy J. 2007;17:343–349
  5. Bradley RL, Arnold E, Barbano DM, Semerad RG, Smith DE, Vines BK. Chemical and physical methods. In:  Marshall R editors. Standard Methods for the Examination of Dairy Products. Washington, DC: Am. Public Health Assoc; 1993;p. 433–531
  6. Bude-Ugarte M, Guglielmotti D, Giraffa G, Reinhemer JA, Hynes E. Nonstarter lactobacilli isolated from soft and semihard argentinean cheeses: Genetic characterization and resistance to biological barriers. J. Food Prot. 2006;69:2983–2991
  7. Capra ML, Quiberoni A, Ackermann H-W, Moineau S, Reinheimer JA. Characterization of a New Virulent Phage (MLC-A) of Lactobacillus paracasei. J. Dairy Sci. 2006;89:2414–2423
  8. Church FC, Swaisgood HE, Porter DH, Catignain GL. Spectrophometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci. 1983;66:1219–1227
  9. Corsetti A, Gobetti M, Smacchi E, De Angelis M, Rossi J. Accelerated ripening of Pecorino Umbro cheese. J. Dairy Res. 1998;65:631–642
  10. Crow VL, Curry B, Hayes M. The ecology of non-starter lactic acid bacteria (NSLAB) and their use as adjuncts in New Zealand Cheddar. Int. Dairy J. 2001;11:275–283
  11. De Angelis M, Corsetti A, Tosti N, Rossi J, Corbo MR, Gobbetti M. Characterization of non-starter lactic acid bacteria from italian ewe cheeses based on phenotypic, genotypic, and cell wall protein analyses. Appl. Environ. Microbiol. 2001;67:2011–2020
  12. Di Cagno R, De Angelis M, Upadhyay V, McSweeney PLH, Minervini F, Gallo G, et al. Effect of proteinases of starter bacteria on the growth and proteolytic activity of Lactobacillus plantarum DPC2741. Int. Dairy J. 2003;13:145–157
  13. Efstathio JD, McKay LL. Plasmids in Streptococcus thermophilus. Evidence that lactose metabolism and proteinase activity are plasmid linked. Appl. Environ. Microbiol. 1976;32:38–44
  14. Fox PF, Law J, McSweeney PLH, Wallace J. Biochemistry of Cheese Ripening. In:  Fox PF editors. Cheese: Chemistry, Physics and Microbiology. Vol. 1:London, UK: Chapman & Hall; 1993;p. 389–438
  15. Fox PF, McSweeney PLH, Lynch CM. Significance of non-starter lactic acid bacteria in Cheddar cheese. Aust. J. Dairy Technol. 1998;53:83–89
  16. Guglielmotti D, Reinheimer JA, Binetti AG, Giraffa G, Carminati D, Quiberoni A. Characterization of spontaneous phage-resistant derivatives of Lactobacillus delbrueckii commercial strains. Int. J. Food Microbiol. 2006;111:126–133
  17. Herreros MA, Arenas R, Sandoval MH, Castro JM, Fresno JM, Tornadijo ME. Effect of addition of native cultures on characteristics of Armada cheese manufactured with pasteurized milk: A preliminary study. Int. Dairy J. 2007;17:328–335
  18. Hynes E, Bergamini CV, Suárez V, Zalazar CA. Proteolysis on Reggianito cheeses manufactured with natural whey cultures and selected strains of Lactobacillus helveticus. J. Dairy Sci. 2003;86:3831–3840
  19. Hynes E, Delacroix-Buchet A, Meinardi CA, Zalazar CA. Relation between pH, degree of proteolysis and consistency in soft cheese. Aust. J. Dairy Technol. 1999;54:24–27
  20. Hynes E, Delacroix-Buchet A, Zalazar CA. Influence of milk-clotting enzyme in proteolysis during ripening of Cremoso Argentino cheese. Aust. J. Dairy Technol. 2001;56:208–212
  21. Hynes E, Ogier J-C, Delacroix-Buchet A. Proteolysis during ripening of miniature washed-curd cheeses manufactured with different strains of starter bacteria and a Lactobacillus plantarum adjunct culture. Int. Dairy J. 2001;11:587–597
  22. International Dairy Federation (IDF). 1982. Determination of the total solid content (cheese and processed cheese). IDF Standard 4A. Brussels, Belgium.
  23. International Dairy Federation (IDF). 1988. Yogurt: Enumeration of characteristic microorganisms. IDF Standard 117A. Brussels, Belgium.
  24. International Dairy Federation (IDF). 1993. Milk. Determination of the nitrogen (Kjeldahl method) and calculation of the crude protein content. IDF Standard 20B. Brussels, Belgium.
  25. International Dairy Federation (IDF). 1997. Lait et produits laitiers. Dtétermination de la teneur en matiére grasse. Guide de directives génerales appliquées aux méthodes butyrometriques. 152A. Brussels, Belgium.
  26. Kieronczyk A, Skeie S, Langsrud T, Yvon M. Cooperation between Lactococcus lactis and nonstarter lactobacilli in the formation of cheese aroma from amino acids. Appl. Environ. Microbiol. 2003;69:734–739
  27. Kleter G. The ripening of Gouda cheese made under strictly aseptic conditions. 2. The comparison of the activity of different starters and the influence of certain Lactobacillus strains. Neth. Milk Dairy J. 1977;31:177–187
  28. Lane CN, Fox PF, Walsh EM, Folkertsma B, McSweeney PLH. Effect of compositional and environmental factors on the growth of indigenous nonstarter lactic acid bacteria in Cheddar cheese. Lait. 1997;77:561–573
  29. Lynch CM, McSweeney PLH, Fox PF, Cogan TM, Drinan FD. Manufacture of Cheddar cheese with and without adjunct lactobacilli under controlled microbiological conditions. Int. Dairy J. 1996;6:851–867
  30. Lynch CM, Muir DD, Banks JM, McSweeney PLH, Fox PF. Influence of adjunct cultures of Lactobacillus paracasei ssp. paracasei or Lactobacillus plantarum on Cheddar cheese ripening. J. Dairy Sci. 1999;82:1618–1628
  31. Macedo AC, Tavares TG, Malcata FX. Influence of native lactic acid bacteria on the microbiological, biochemical and sensory profiles of Serra da Estrela cheese. Food Microbiol. 2004;21:233–240
  32. Macedo AC, Vieira M, Poças R, Malcata FX. Peptide hydrolase system of lactic acid bacteria isolated from Serra da Estrela cheese. Int. Dairy J. 2000;10:769–774
  33. Martínez-Cuesta MC, Fernández de Palencia P, Requena T, Peláez C. Enzymatic ability of Lactobacillus casei subsp. casei IFPL731 for flavour development in cheese. Int. Dairy J. 2001;11:577–585
  34. Martley FG, Crow VL. Interaction between nonstarter microorganisms during cheese manufacture and ripening. Int. Dairy J. 1993;3:461–483
  35. McKay LL, Baldwin KA. Simultaneous loss of proteinase and lactose utilizing enzymes activities in Lactococcus and reversal of loss by transduction. Am. Soc. Microbiol. 1974;20:342–346
  36. McSweeney PLH, Walsh EM, Fox PF, Cogan TM, Drinan FD, Castelo-Gonzalez M. A procedure for the manufacture of Cheddar cheese under controlled bacteriological conditions and the effect of adjunct lactobacilli on cheese quality. Irish J. Agric. Food Res. 1994;33:183–192
  37. Mendia C, Iban→ez FJ, Torre P, Barcina Y. Effect of pasteurization and use of a native starter culture on proteolysis in a ewes’ milk cheese. Food Contr. 2000;11:195–200
  38. Mercanti DJ, Milesi MM, Hynes E. Fermentos de lactobacilos mesófilos para quesería. In: Proc. 9° Congresso Panamericano do Leite, FEPALE. Brazil.: Porto Alegre; 2006;p. 381–385
  39. Moineau S, Lévesque C. Control of bacteriophages in industrial fermentations. In:  Kutter E,  Sulakvelidze A editor. Bacteriophages: Biology and Applications. Boca Raton, FL: CRC Press; 2005;p. 285–296
  40. Naylor J, Sharpe ME. Lactobacilli in Cheddar cheese. III. The source of lactobacilli in cheese. J. Dairy Res. 1958;25:431–438
  41. Peterson SD, Marshall RT. Nonstarter lactobacilli in Cheddar cheese: A review. J. Dairy Sci. 1990;73:1395–1410
  42. Quiberoni A, Tailliez P, Quénee P, Suárez V, Reinheimer JA. Genetic (RAPD-PCR) and technological diversities among wild Lactobacillus helveticus strains. J. Appl. Microbiol. 1998;85:591–596
  43. Reddy KA, Marth EH. Proteolysis in cheddar cheese made with sodium chloride, potassium chloride or mixtures of sodium and potassium chloride. Lebensm. Wiss. Technol. 1993;26:434–442
  44. Sánchez I, Seseña S, Poveda JM, Cabezas L, Palop L. Genetic diversity, dynamics, and activity of Lactobacillus community involved in traditional processing of artisanal Manchego cheese. Int. J. Food Microbiol. 2006;107:265–273
  45. Shakeel-Ur-Rehman J, Banks M, Brechany EY, Muir DD, McSweeney PLH, Fox PF. Influence of ripening temperature on the volatiles and flavour of Cheddar cheese made from raw or pasteurised milk. Int. Dairy J. 2000;10:55–65
  46. Shakeel-Ur-Rehman J, Banks M, McSweeney PLH, Fox PF. Effect of ripening temperature on the growth and significance of non-starter acid bacteria in Cheddar cheese made from raw or pasteurised milk. Int. Dairy J. 2000;10:45–53
  47. Shakeel-Ur-Rehman P, Fox F, McSweeney PLH. Methods used to study non-starter microorganisms in cheese: A review. Int. J. Dairy Technol. 2000;53:113–119
  48. Somers EB, Johnson ME, Wong ACL. Biofilm formation and contamination of cheese by nonstarter lactic acid bacteria in the dairy environment. J. Dairy Sci. 2000;84:1926–1936
  49. Stanley G. Microbiology of fermented milk products. In:  Early R editors. The Technology of Dairy Products. London, UK: Blackie Academic & Professional; 1998;p. 50–79
  50. Svensson U, Christiansson A. Methods for phage monitoring. 263. Brussels, Belgium: Bulletin Int. Dairy Fed. (IDF); 1991;29–39
  51. Swearingen PA, O'Sullivan DJ, Warthsehen JJ. Isolation, characterisation and influence of native, nonstarter lactic acid bacteria on Cheddar cheese quality. J. Dairy Sci. 2001;84:50–59
  52. Thage BV, Broe ML, Petersen MH, Petersen MA, Bennedsen M, Ardö Y. Aroma development in semihard reduced-fat cheese inoculated with Lactobacillus casei with different aminotransferase profiles. Int. Dairy J. 2005;15:795–805
  53. Thomas T. Cannibalism among bacteria found in cheese. N. Z. J. Dairy Sci. Technol. 1987;22:215–219
  54. Turner KW, Lawrence RC, Lelievre J. A microbiological specification for milk for aseptic cheese making. N. Z. J. Dairy Sci. Technol. 1986;21:249–254
  55. Vinderola CG, Reinheimer JA. Enumeration of Lactobacillus casei in the presence of Lactobacillus acidophilus, bifidobacteria and lactic starter bacteria in fermented dairy products. Int. Dairy J. 2000;10:271–275
  56. Williams AG, Banks JM. Proteolytic and other hydrolytic enzyme activities in non-starter lactic acid bacteria (NSLAB) isolated from Cheddar cheese manufactured in the United Kingdom. Int. Dairy J. 1997;7:763–774
  57. Williams AG, Noble J, Tammam J, Lloyd D, Banks JM. Factors affecting the activity of enzymes involved in peptide and amino acid catabolism in non-starter lactic acid bacteria isolated from Cheddar cheese. Int. Dairy J. 2002;12:841–852
  58. Williams AG, Withers SE, Banks JM. Energy sources of non starter lactic acid bacteria isolated from Cheddar cheese. Int. Dairy J. 2000;10:17–23
  59. Yvon M. Key enzymes for flavour formation by lactic acid bacteria. Aust. J. Dairy Technol. 2006;61:16–24

PII: S0022-0302(07)71917-3

doi: 10.3168/jds.2007-0180

Journal of Dairy Science
Volume 90, Issue 10 , Pages 4532-4542 , October 2007