Storing Lactic Acid Bacteria: Current Methodologies and Physiological Implications

  • Chalat Santivarangkna
  • Ulrich Kulozik
  • Petra Foerst
Part of the Food Microbiology and Food Safety book series (FMFS)


The high viability of lactic acid bacteria (LAB) during storage is greatly important for starter cultures used for the direct inoculation to food matrices and for the development of probiotic products. The established methods for preservation are freezing and freeze-drying, in which cells are maintained in frozen and dried forms. The frozen cells should be kept at a low storage temperature, such as −80°C, and rapid thawing is recommended for cells frozen with liquid nitrogen. The dried cells should have a low moisture content (<4%). They should be stored at a low relative humidity and temperature and rehydrated in a warm rehydration medium. In addition to these established methodologies, dried cells can be prepared by alternative drying processes such as spray-, fluidized bed-, and vacuum-drying. The viability of frozen and dried cells can be improved by the addition of protectants such as skim milk and sugars. The physiological state of LAB plays a crucial role, and an increased viability can be obtained by the sublethal stress treatment of cells. Exposing LAB cells to a mild stress triggers cells’ protective mechanisms to subsequent stresses occurring during the preservation processes. These stresses are, for example, the entry of cells to the stationary phase; osmotic, heat, cold, and acid shock; as well as genetic modification of genes related to those stresses.


Lactic Acid Bacterium Starter Culture Cold Shock Compatible Solute High Viability 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aguilera JM, Karel M (1997) Preservation of biological materials under desiccation. Crit Rev Food Sci Nutr 37:287–309CrossRefGoogle Scholar
  2. Ananta E, Volkert M, Knorr D (2005) Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus GG. Int Dairy J 15:399–409CrossRefGoogle Scholar
  3. Andersen AB, Fog-Peterson MS, Larsen H, Skibsted LH (1999) Storage stability of freeze-dried starter cultures (Streptococcus thermophilus) as related to physical state of freezing matrix. Food Sci Technol 32:540–547Google Scholar
  4. Baati L, Fabre-Gea C, Auriol D, Blanc PJ (2000) Study of the cryotolerance of Lactobacillus acidophilus: effect of culture and freezing conditions on the viability and cellular protein levels. Int J Food Microbiol 59:241–247CrossRefGoogle Scholar
  5. Baumann DP, Reinbold GW (1966) Freezing of lactic cultures. J Dairy Sci 49:259–264CrossRefGoogle Scholar
  6. Beal C, Corrieu G (1994) Viability and acidification activity of pure and mixed starters of Streptococcus salivarius ssp thermophilus-404 and Lactobacillus delbrueckii ssp bulgaricus-398 at the different steps of their production. Food Sci Technol 27:86–92Google Scholar
  7. Beal C, Fonseca F, Corrieu G (2001) Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J Dairy Sci 84:2347–2356CrossRefGoogle Scholar
  8. Beaufils S, Sauvageot N, Maze A, Laplace JM, Auffray Y, Deutscher J, Hartke A (2007) The cold shock response of Lactobacillus casei: relation between HPr phosphorylation and resistance to freeze/thaw cycles. J Mol Microbiol Biotechnol 13:65–75CrossRefGoogle Scholar
  9. Bielecka M, Majkowska A (2000) Effect of spray drying temperature of yoghurt on the survival of starter cultures, moisture content and sensoric properties of yoghurt powder. Nahrung-Food 44:257–260CrossRefGoogle Scholar
  10. Brennan M, Wanismail B, Johnson MC, Ray B (1986) Cellular-damage in dried Lactobacillus acidophilus. J Food Prot 49:47–53Google Scholar
  11. Broadbent JR, Lin C (1999) Effect of heat shock or cold shock treatment on the resistance of Lactococcus lactis to freezing and lyophilization. Cryobiology 39:88–102CrossRefGoogle Scholar
  12. Brown AD (1976) Microbial water stress. Bacteriol Rev 40:803–846Google Scholar
  13. Carcoba R, Rodriguez A (2000) Influence of cryoprotectants on the viability and acidifying activity of frozen and freeze-dried cells of the novel starter strain Lactococcus lactis ssp lactis CECT 5180. Eur Food Res Technol 211:433–437CrossRefGoogle Scholar
  14. Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, Gibbs P (2002) Survival of freeze-dried Lactobacillus plantarum and Lactobacillus rhamnosus during storage in the presence of protectants. Biotechnol Lett 24:1587–1591CrossRefGoogle Scholar
  15. Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, Gibbs P (2003a) Effects of addition of sucrose and salt, and of starvation upon thermotolerance and survival during storage of freeze-dried Lactobacillus delbrueckii ssp. bulgaricus. J Food Sci 68:2538–2541CrossRefGoogle Scholar
  16. Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, Gibbs P (2003b) Protective effect of sorbitol and monosodium glutamate during storage of freeze-dried lactic acid bacteria. Lait 83:203–210CrossRefGoogle Scholar
  17. Castro HP, Teixeira P, Kirby R (1995) Storage of lyophilized cultures of Lactobacillus bulgaricus under different relative humidities and atmospheres. Appl Microbiol Biotechnol 44:172–176CrossRefGoogle Scholar
  18. Castro HP, Teixeira PM, Kirby R (1996) Changes in the cell membrane of Lactobacillus bulgaricus during storage following freeze-drying. Biotechnol Lett 18:99–104CrossRefGoogle Scholar
  19. Champagne CP, Gardner N, Brochu E, Beaulieu Y (1991) The freeze drying of lactic acid bacteria – a review. Can Inst Food Sci Technol J 24:118–128Google Scholar
  20. Chou LS, Weimer B (1999) Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. J Dairy Sci 82:23–31CrossRefGoogle Scholar
  21. Clementi F, Rossi J (1984) Effect of drying and storage conditions on survival of Leuconostoc oenos. Am J Enol Vitic 35:183–186Google Scholar
  22. Conrad PB, Miller DP, Cielenski PR, de Pablo JJ (2000) Stabilization and preservation of Lactobacillus acidophilus in saccharide matrices. Cryobiology 41:17–24CrossRefGoogle Scholar
  23. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C (2004) Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J Appl Microbiol 96:1024–1039CrossRefGoogle Scholar
  24. Coulibaly I, Amenan AY, Lognay G, Fauconnier ML, Thonart P (2009) Survival of freeze-dried Leuconostoc mesenteroides and Lactobacillus plantarum related to their cellular fatty acids composition during storage. Appl Biochem Biotechnol 157:70–84CrossRefGoogle Scholar
  25. Crowe JH, Crowe LM, Mouradian R (1983) Stabilization of biological membranes at low water activities. Cryobiology 20:346–356CrossRefGoogle Scholar
  26. De Angelis M, Gobbetti M (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4:106–122CrossRefGoogle Scholar
  27. De Antoni GL, Perez P, Abraham A, Anon MC (1989) Trehalose, a cryoprotectant for Lactobacillus bulgaricus. Cryobiology 26:149–153CrossRefGoogle Scholar
  28. De Urraza P, De Antoni G (1997) Induced cryotolerance of Lactobacillus delbrueckii supsp. bulgaricusb LBB by preincubation at suboptimal temperatures with a fermentable sugar. Cryobiology 35:159–164CrossRefGoogle Scholar
  29. De Valdez GF (2001) Maintenance of lactic acid bacteria. In: Spencer JFT, De Spencer ALG (Eds.), Food microbiology protocols. Humana Press, Totawa, pp. 163–172Google Scholar
  30. De Valdez GF, Degiori GS, Holgado APD, Oliver G (1985) Effect of the rehydration medium on the recovery of freeze dried lactic acid bacteria. Appl Environ Microbiol 50:1339–1341Google Scholar
  31. Derzelle S, Hallet B, Francis KP, Ferain T, Delcour J, Hols P (2000) Changes in cspL, cspP, and cspC mRNA abundance as a function of cold shock and growth phase in Lactobacillus plantarum. J Bacteriol 182:5105–5113CrossRefGoogle Scholar
  32. Derzelle S, Hallet B, Ferain T, Delcour J, Hols P (2003) Improved adaptation to cold-shock, ­stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Appl Environ Microbiol 69:4285–4290CrossRefGoogle Scholar
  33. Desmond C, Ross RP, O’Callaghan E, Fitzgerald G, Stanton C (2002a) Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia. J Appl Microbiol 93:1003–1011CrossRefGoogle Scholar
  34. Desmond C, Stanton C, Fitzgerald GF, Collins K, Ross RP (2002b) Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int Dairy J 12:183–190CrossRefGoogle Scholar
  35. Desmond C, Fitzgerald GF, Stanton C, Ross RP (2004) Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl Environ Microbiol 70:5929–5936CrossRefGoogle Scholar
  36. Dumont F, Marechal PA, Gervais P (2004) Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Appl Environ Microbiol 70:268–272CrossRefGoogle Scholar
  37. Duong T, Barrangou R, Russell WM, Klaenhammer TR (2006) Characterization of the tre locus and analysis of trehalose cryoprotection in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 72:1218–1225CrossRefGoogle Scholar
  38. Efiuvwevwere BJO, Gorris LGM, Smid EJ, Kets EPW (1999) Mannitol-enhanced survival of Lactococcus lactis subjected to drying. Appl Microbiol Biotechnol 51:100–104CrossRefGoogle Scholar
  39. Fernandez A, Varez-Ordonez A, Lopez M, Bernardo A (2009) Effects of organic acids on thermal inactivation of acid and cold stressed Enterococcus faecium. Food Microbiol 26:497–503CrossRefGoogle Scholar
  40. Fonseca F, Beal C, Corrieu G (2000) Method of quantifying the loss of acidification activity of lactic acid starters during freezing and frozen storage. J Dairy Res 67:83–90CrossRefGoogle Scholar
  41. Fonseca F, Beal C, Corrieu G (2001) Operating conditions that affect the resistance of lactic acid bacteria to freezing and frozen storage. Cryobiology 43:189–198CrossRefGoogle Scholar
  42. Fonseca F, Marin M, Morris GJ (2006) Stabilization of frozen Lactobacillus delbrueckii subsp. bulgaricus in glycerol suspensions: freezing kinetics and storage temperature effects. Appl Environ Microbiol 72:6474–6482CrossRefGoogle Scholar
  43. Foschino R, Fiori E, Galli A (1996) Survival and residual activity of Lactobacillus acidophilus frozen cultures under different conditions. J Dairy Res 63:295–303CrossRefGoogle Scholar
  44. Gardiner GE, O’Sullivan E, Kelly J, Auty MA, Fitzgerald GF, Collins JK, Ross RP, Stanton C (2000) Comparative survival rates of human-derived probiotic Lactobacillus paracasei and L. salivarius strains during heat treatment and spray drying. Appl Environ Microbiol 66:2605–2612CrossRefGoogle Scholar
  45. Gehrke H (1991) Untersuchungen zur Gefriertrocknung von Mikroorganismen [in German]. Dissertation, Universität BraunschweigGoogle Scholar
  46. Giard JC, Hartke A, Flahaut S, Benachour A, Boutibonnes P, Auffray Y (1996) Starvation-induced multiresistance in Enterococcus faecalis JH2–2. Curr Microbiol 32:264–271CrossRefGoogle Scholar
  47. Glaasker E, Konings WN, Poolman B (1996) Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J Bacteriol 178:575–582Google Scholar
  48. Glaasker E, Tjan FSB, Ter Steeg PF, Konings WN, Poolman B (1998) Physiological response of Lactobacillus plantarum to salt and nonelectrolyte stress. J Bacteriol 180:4718–4723Google Scholar
  49. Grout BWW, Morris GJ (2008) Contaminated liquid nitrogen storage vessels as potential vectors for pathogens. Cryo-Lett 29:74–75Google Scholar
  50. Grout BWW, Morris GJ (2009) Contaminated liquid nitrogen vapour as a risk factor in pathogen transfer. Theriogenology 71:1079–1082CrossRefGoogle Scholar
  51. Heckly RJ (1961) Preservation of bacteria by lyophilization. Adv Appl Microbiol 3:1–76CrossRefGoogle Scholar
  52. Higl B, Kurtmann L, Carlsen CU, Ratjen J, Forst P, Skibsted LH, Kulozik U, Risbo J (2007) Impact of water activity, temperature, and physical state on the storage stability of Lactobacillus paracasei ssp. paracasei freeze-dried in a lactose matrix. Biotechnol Prog 23:794–800Google Scholar
  53. Higl B, Santivarangkna C, Foerst P (2008) Bewertung und Optimierung von Gefrier-und Vakuumtrocknungsverfahren in der Herstellung von mikrobiellen Starterkulturen [in German]. Chemie Inginieur Technik 80: 1157–1164CrossRefGoogle Scholar
  54. Hua L, Zhao WY, Wang H, Li ZC, Wang AL (2009) Influence of culture pH on freeze-drying viability of Oenococcus oeni and its relationship with fatty acid composition. Food Bioprod Process 87:56–61CrossRefGoogle Scholar
  55. Hubalek Z (2003) Protectants used in the cryopreservation of microorganisms. Cryobiology 46:205–229CrossRefGoogle Scholar
  56. Hutkins RW, Ellefson WL, Kashket ER (1987) Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus. Appl Environ Microbiol 53:2275–2281Google Scholar
  57. Jewell JB, Kashket ER (1991) Osmotically regulated transport of proline by Lactobacillus acidophilus IFO 3532. Appl Environ Microbiol 57:2829–2833Google Scholar
  58. Johannsen E (1972) Influence of various factors on the survival of Lactobacillus leichmannii during freezing and thawing. J Appl Bacteriol 35:415–421Google Scholar
  59. Juarez TMS, Ocana VS, Nader-Macias ME (2004) Viability of vaginal probiotic lactobacilli during refrigerated and frozen storage. Anaerobe 10:1–5CrossRefGoogle Scholar
  60. Juarez TMS, Bru E, Martos G, Nader-Macias ME (2009) Stability of freeze-dried vaginal Lactobacillus strains in the presence of different lyoprotectors. Can J Microbiol 55:544–552CrossRefGoogle Scholar
  61. Keogh BP (1970) Survival and activity of frozen starter cultures for cheese manufacture. Appl Microbiol 19:928–931Google Scholar
  62. Kets EPW, De Bont JAM (1994) Protective effect of betaine on survival of Lactobacillus plantarum subjected to drying. FEMS Microbiol Lett 116:251–255CrossRefGoogle Scholar
  63. Kets EPW, Teunissen PJM, De Bont JAM (1996) Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Appl Environ Microbiol 62:259–261Google Scholar
  64. Kets EPW, Groot MN, Galinski EA, De Bont JAM (1997) Choline and acetylcholine: novel cationic osmolytes in Lactobacillus plantarum. Appl Microbiol Biotechnol 48:94–98CrossRefGoogle Scholar
  65. Kilimann KV, Doster W, Vogel RF, Hartmann C, Ganzle MG (2006) Protection by sucrose against heat-induced lethal and sublethal injury of Lactococcus lactis: an FT-IR study. Biochim Biophys Acta 1764:1188–1197Google Scholar
  66. Kilstrup M, Jacobsen S, Hammer K, Vogensen FK (1997) Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress is Lactococcus lactis. Appl Environ Microbiol 63:1826–1837Google Scholar
  67. Kim SJ, Kim JH, Park JY, Kim HT, Jeong SJ, Ha YL, Yun HD, Kim JH (2004) Cold adaptation of Lactobacillus paraplantarum C7 isolated from kimchi. J Microbiol Biotechnol 14:1071–1074Google Scholar
  68. Kim SS, Bhowmik SR (1990) Survival of lactic acid bacteria during spray drying of plain yogurt. J Food Sci 55:1008–1011CrossRefGoogle Scholar
  69. Kim WS, Dunn NW (1997) Identification of a cold shock gene in lactic acid bacteria and the effect of cold shock on cryotolerance. Curr Microbiol 35:59–63CrossRefGoogle Scholar
  70. Kim WS, Khunajakr N, Dunn NW (1998) Effect of cold shock on protein synthesis and on cryotolerance of cells frozen for long periods in Lactococcus lactis. Cryobiology 37:86–91CrossRefGoogle Scholar
  71. Kim WS, Ren J, Dunn NW (1999) Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol Lett 171:57–65CrossRefGoogle Scholar
  72. King VAE, Su JT (1993) Dehydration of Lactobacillus acidophilus. Proc Biochem 28:47–52CrossRefGoogle Scholar
  73. King VAE, Lin HJ, Liu CF (1998) Accelerated storage testing of freeze-dried and controlled low-temperature vacuum dehydrated Lactobacillus acidophilus. J Gen Appl Microbiol 44:161–165CrossRefGoogle Scholar
  74. Knorr D (1998) Technology aspects related to microorganisms in functional foods. Trends Food Sci Technol 9:295–306CrossRefGoogle Scholar
  75. Kurtmann L, Carlsen CU, Risbo J, Skibsted LH (2009a) Storage stability of freeze-dried Lactobacillus acidophilus (La-5) in relation to water activity and presence of oxygen and ascorbate. Cryobiology 58:175–180CrossRefGoogle Scholar
  76. Kurtmann L, Carlsen CU, Skibsted LH, Risbo J (2009b) Water activity-temperature state diagrams of freeze-dried Lactobacillus acidophilus (La-5): influence of physical state on bacterial survival during storage. Biotechnol Prog 25:265–270CrossRefGoogle Scholar
  77. Kurtmann L, Skibsted LH, Carlsen CU (2009c) Browning of freeze-dried probiotic bacteria cultures in relation to loss of viability during storage. J Agric Food Chem 57:6736–6741CrossRefGoogle Scholar
  78. Le MC, Bon E, Lonvaud-Funel A (2007) Tolerance to high osmolality of the lactic acid bacterium Oenococcus oeni and identification of potential osmoprotectants. Int J Food Microbiol 115:335–342CrossRefGoogle Scholar
  79. Lee K (2004) Cold shock response in Lactococcus lactis ssp. diacetylactis: a comparison of the protection generated by brief pre-treatment at less severe temperatures. Proc Biochem 39:2233–2239CrossRefGoogle Scholar
  80. Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM (1995) Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol 61:3592–3597Google Scholar
  81. Lian WC, Hsiao HC, Chou CC (2002) Survival of bifidobacteria after spray-drying. Int J Food Microbiol 74:79–86CrossRefGoogle Scholar
  82. Linders LJM, Meerdink G, Vantriet K (1997a) Effect of growth parameters on the residual activity of Lactobacillus plantarum after drying. J Appl Microbiol 82:683–688CrossRefGoogle Scholar
  83. Linders LJM, Wolkers WF, Hoekstra FA, Vantriet K (1997b) Effect of added carbohydrates on membrane phase behavior and survival of dried Lactobacillus plantarum. Cryobiology 35:31–40CrossRefGoogle Scholar
  84. Lorca GL, De Valdez GF (1998) Temperature adaptation and cryotolerance in Lactobacillus acidophilus. Biotechnol Lett 20:847–849CrossRefGoogle Scholar
  85. Mauriello G, Aponte M, Andolfi R, Moschetti G, Villani F (1999) Spray-drying of bacteriocin-producing lactic acid bacteria. J Food Prot 62:773–777Google Scholar
  86. Mazur P (1970) Cryobiology – freezing of biological systems. Science 168:939–949CrossRefGoogle Scholar
  87. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:C125-C142Google Scholar
  88. Melin AM, Perromat A, Deleris G (1999) Pharmacologic application of FTIR spectroscopy: effect of ascorbic acid-induced free radicals on Deinococcus radiodurans. Biospectroscopy 5:229–236CrossRefGoogle Scholar
  89. Mille Y, Obert JP, Beney L, Gervais P (2004) New drying process for lactic bacteria based on their dehydration behavior in liquid medium. Biotechnol Bioeng 88:71–76CrossRefGoogle Scholar
  90. Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, Nakahara T (2006) Survival curves for microbial species stored by freeze-drying. Cryobiology 52:27–32CrossRefGoogle Scholar
  91. Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, Nakahara T (2008) Survival of freeze-dried bacteria. J Gen Appl Microbiol 54:9–24CrossRefGoogle Scholar
  92. Modesto M, Mattarelli P, Biavati B (2004) Resistance to freezing and freeze-drying storage processes of potential probiotic bifidobacteria. Ann Microbiol 54:43–48Google Scholar
  93. Monnet C, Beal C, Corrieu G (2003) Improvement of the resistance of Lactobacillus delbrueckii ssp. bulgaricus to freezing by natural selection. J Dairy Sci 86:3048–3053CrossRefGoogle Scholar
  94. Morice M, Bracquart P, Linden G (1992) Colonial variation and freeze-thaw resistance of Streptococcus thermophilus. J Dairy Sci 75:1197–1203CrossRefGoogle Scholar
  95. Morris GJ (2005) The origin, ultrastructure, and microbiology of the sediment accumulating in liquid nitrogen storage vessels. Cryobiology 50:231–238CrossRefGoogle Scholar
  96. Nakamura LK (1996) Preservation and maintenance of eubacteria. In: Hunter-Cevera JC, Belt A (Eds.), Maintaining cultures for biotechnology and industry. Academic, London, pp. 65–84Google Scholar
  97. Obis D, Guillot A, Mistou MY (2001) Tolerance to high osmolality of Lactococcus lactis subsp. lactis and cremoris is related to the activity of a betaine transport system. FEMS Microbiol Lett 202:39–44CrossRefGoogle Scholar
  98. Panoff JM, Thammavongs B, Laplace JM, Hartke A, Boutibonnes P, Auffray Y (1995) Cryotolerance and cold adaptation in Lactococcus lactis subsp lactis IL1403. Cryobiology 32:516–520CrossRefGoogle Scholar
  99. Panoff JM, Thammavongs B, Gueguen M (2000) Cryoprotectants lead to phenotypic adaptation to freeze-thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40:264–269CrossRefGoogle Scholar
  100. Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917–925CrossRefGoogle Scholar
  101. Rivals JP, Beal C, Thammavongs B, Gueguen M, Panoff JM (2007) Cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1 is modified by acquisition of antibiotic resistance. Cryobiology 55:19–26CrossRefGoogle Scholar
  102. Roelans E, Taeymans D (1990) Effect of drying conditions on survival and enzyme activity of microorganims. In: Spiess WEL, Schubert H (Eds.), Engineering and food, Vol. 3: advanced processes. Elsevier Applied Science, London, pp. 559–569Google Scholar
  103. Sanders JW, Venema G, Kok J (1999) Environmental stress responses in Lactococcus lactis. FEMS Microbiol Rev 23:483–501CrossRefGoogle Scholar
  104. Sandine WE (1996) Commercial production of dairy starter cultures. In: Cogan TM, Accolas JP (Eds.), Dairy starter cultures. VCH, New York, pp. 191–206Google Scholar
  105. Santivarangkna C, Kulozik U, Foerst P (2006) Effect of carbohydrates on the survival of Lactobacillus helveticus during vacuum drying. Lett Appl Microbiol 42:271–276CrossRefGoogle Scholar
  106. Santivarangkna C, Wenning M, Foerst P, Kulozik U (2007) Damage of cell envelope of Lactobacillus helveticus during vacuum drying. J Appl Microbiol 102:748–756CrossRefGoogle Scholar
  107. Santivarangkna C, Higl B, Foerst P (2008) Protection mechanisms of sugars during different stages of preparation process of dried lactic acid starter cultures. Food Microbiol 25:429–441CrossRefGoogle Scholar
  108. Schoug A, Fischer J, Heipieper HJ, Schnurer J, Hakansson S (2008) Impact of fermentation pH and temperature on freeze-drying survival and membrane lipid composition of Lactobacillus coryniformis Si3. J Ind Microbiol Biotechnol 35:175–181CrossRefGoogle Scholar
  109. Schweigart F (1971) The drying of lactic acid bacteria cultures for Mahewu production. Lebensmittel-Wissenschaft und -Technologie 4:20–23Google Scholar
  110. Selmer-Olsen E, Birkeland SE, Sorhaug T (1999a) Effect of protective solutes on leakage from and survival of immobilized Lactobacillus subjected to drying, storage and rehydration. J Appl Microbiol 87:429–437CrossRefGoogle Scholar
  111. Selmer-Olsen E, Sorhaug T, Birkeland SE, Pehrson R (1999b) Survival of Lactobacillus helveticus entrapped in Ca-alginate in relation to water content, storage and rehydration. J Ind Microbiol Biotechnol 23:79–85CrossRefGoogle Scholar
  112. Serror P, Dervyn R, Ehrlich SD, Maguin E (2003) csp-like genes of Lactobacillus delbrueckii ssp. bulgaricus and their response to cold shock. FEMS Microbiol Lett 226:323–330CrossRefGoogle Scholar
  113. Sheehan VM, Sleator RD, Fitzgerald GF, Hill C (2006) Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:2170–2177CrossRefGoogle Scholar
  114. Silva J, Carvalho AS, Teixeira P, Gibbs PA (2002) Bacteriocin production by spray-dried lactic acid bacteria. Lett Appl Microbiol 34:77–81CrossRefGoogle Scholar
  115. Silva J, Carvalho AS, Pereira H, Teixeira P, Gibbs PA (2004) Induction of stress tolerance in Lactobacillus delbrueckii ssp. bulgaricus by the addition of sucrose to the growth medium. J Dairy Res 71:121–125CrossRefGoogle Scholar
  116. Silva J, Carvalho AS, Ferreira R, Vitorino R, Amado F, Domingues P, Teixeira P, Gibbs PA (2005) Effect of the pH of growth on the survival of Lactobacillus delbrueckii subsp. bulgaricus to stress conditions during spray-drying. J Appl Microbiol 98:775–782CrossRefGoogle Scholar
  117. Sinha RN, Dudani AT, Ranganathan B (1974) Protective effect of fortified skim milk as suspending medium for freeze drying of different lactic acid bacteria. J Food Sci 39:641–642CrossRefGoogle Scholar
  118. Strasser S, Neureiter M, Geppl M, Braun R, Danner H (2009) Influence of lyophilization, fluidized bed drying, addition of protectants, and storage on the viability of lactic acid bacteria. J Appl Microbiol 107:167–177CrossRefGoogle Scholar
  119. Streit F, Corrieu G, Beal C (2007) Acidification improves cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1. J Biotechnol 128:659–667CrossRefGoogle Scholar
  120. Streit F, Delettre J, Corrieu G, Beal C (2008) Acid adaptation of Lactobacillus delbrueckii subsp. bulgaricus induces physiological responses at membrane and cytosolic levels that improves cryotolerance. J Appl Microbiol 105:1071–1080CrossRefGoogle Scholar
  121. Succi M, Tremonte P, Reale A, Sorrentino E, Coppola R (2007) Preservation by freezing of potentially probiotic strains of Lactobacillus rhamnosus. Ann Microbiol 57:537–544CrossRefGoogle Scholar
  122. Sunny-Roberts EO, Knorr D (2007) Physiological analysis of Lactobacillus rhamnosus VTT E-97800 – adaptive response to osmotic stress induced by trehalose. Br Food J 109:735–748CrossRefGoogle Scholar
  123. Sunny-Roberts EO, Knorr D (2008) Evaluation of the response of Lactobacillus rhamnosus VTT E-97800 to sucrose-induced osmotic stress. Food Microbiol 25:183–189CrossRefGoogle Scholar
  124. Sunny-Roberts EO, Knorr D (2009) The protective effect of monosodium glutamate on survival of Lactobacillus rhamnosus GG and Lactobacillus rhamnosus E-97800 (E800) strains during spray-drying and storage in trehalose-containing powders. Int Dairy J 19:209–214CrossRefGoogle Scholar
  125. Teixeira P, Castro H, Kirby R (1993) Inducible thermotolerance in Lactobacillus bulgaricus. Lett Appl Microbiol 18:218–221CrossRefGoogle Scholar
  126. Teixeira P, Castro H, Kirby R (1995a) Spray drying as a method for preparing concentrated cultures of Lactobacillus bulgaricus. J Appl Bacteriol 78:456–462Google Scholar
  127. Teixeira PC, Castro MH, Malcata FX, Kirby RM (1995b) Survival of Lactobacillus delbrueckii ssp. bulgaricus following spray-drying. J Dairy Sci 78:1025–1031CrossRefGoogle Scholar
  128. Teixeira P, Castro H, Kirby R (1996) Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett Appl Microbiol 22:34–38CrossRefGoogle Scholar
  129. Termont S, Vandenbroucke K, Iserentant D, Neirynck S, Steidler L, Remaut E, Rottiers P (2006) Intracellular accumulation of trehalose protects Lactococcus lactis from freeze-drying damage and bile toxicity and increases gastric acid resistance. Appl Environ Microbiol 72:7694–7700CrossRefGoogle Scholar
  130. Thunell RK, Sandine WE, Bodyfelt FW (1984) Frozen starters from internal pH control grown cultures. J Dairy Sci 67:24–36CrossRefGoogle Scholar
  131. To BCS, Etzel MR (1997) Spray drying, freeze drying, or freezing of three different lactic acid bacteria species. J Food Sci 62:576–585CrossRefGoogle Scholar
  132. Tsvetkov T, Brankova R (1983) Viability of micrococci and lactobacilli upon freezing and freeze drying in the presence of different cryoprotectants. Cryobiology 20:318–323CrossRefGoogle Scholar
  133. Tsvetkov T, Shishkova I (1982) Studies on the effects of low temperatures on lactic acid bacteria. Cryobiology 19:211–214CrossRefGoogle Scholar
  134. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie von Leeuwenhoek 82:187–216CrossRefGoogle Scholar
  135. Varcamonti M, Arsenijevic S, Martirani L, Fusco D, Naclerio G, De Felice M (2006) Expression of the heat shock gene ClpL of Streptococcus thermophilus is induced by both heat and cold shock. Microb Cell Fact. doi:  10.1186/1475–2859–5-6
  136. Volkert M, Ananta E, Luscher C, Knorr D (2008) Effect of air freezing, spray freezing, and pressure shift freezing on membrane integrity and viability of Lactobacillus rhamnosus GG. J Food Eng 87:532–540Google Scholar
  137. Walker DC, Girgis HS, Klaenhammer TR (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl Environ Microbiol 65:3033–3041Google Scholar
  138. Wang YC, Yu RC, Chou CC (2004) Viability of lactic acid bacteria and bifidobacteria in fermented soymilk after drying, subsequent rehydration and storage. Int J Food Microbiol 93:209–217CrossRefGoogle Scholar
  139. Wang Y, Corrieu G, Beal C (2005) Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J Dairy Sci 88:21–29CrossRefGoogle Scholar
  140. Welsh DT, Herbert RA (1999) Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. FEMS Microbiol Lett 174:57–63CrossRefGoogle Scholar
  141. Wolfe J (1987) Lateral stresses in membranes at low water potential. Aust J Plant Physiol 14:311–318CrossRefGoogle Scholar
  142. Wolff E, Louvet P, Gilbert H (1986) Atmospheric freeze drying: design and energy considerations. In: Arun S, Mujumdar (Eds.), Drying’86. 5th International Symposium on Drying, Cambridge, MA, August. Hemisphere Publishing, Washington, pp. 432–439Google Scholar
  143. Wolff E, Delisle B, Corrieu G, Gibert H (1990) Freeze-drying of Streptococcus thermophilus: a comparison between the vacuum and the atmospheric method. Cryobiology 27:569–575CrossRefGoogle Scholar
  144. Wouters JA, Jeynov B, Rombouts FM, De Vos WM, Kuipers OP, Abee T (1999a) Analysis of the role of 7 kDa cold-shock proteins of Lactococcus lactis MG1363 in cryoprotection. Microbiology 145:3185–3194Google Scholar
  145. Wouters JA, Rombouts FM, De Vos WM, Kuipers OP, Abee T (1999b) Cold shock proteins and low-temperature response of Streptococcus thermophilus CNRZ302. Appl Environ Microbiol 65:4436–4442Google Scholar
  146. Wouters JA, Mailhes M, Rombouts FM, De Vos WM, Kuipers OP, Abee T (2000) Physiological and regulatory effects of controlled overproduction of five cold shock proteins of Lactococcus lactis MG1363. Appl Environ Microbiol 66:3756–3763CrossRefGoogle Scholar
  147. Yao AA, Coulibaly I, Lognay G, Fauconnier ML, Thonart P (2008) Impact of polyunsaturated fatty acid degradation on survival and acidification activity of freeze-dried Weissella paramesenteroides LC11 during storage. Appl Microbiol Biotechnol 79:1045–1052CrossRefGoogle Scholar
  148. Zhao G, Zhang G (2005) Effect of protective agents, freezing temperature, rehydration media on viability of malolactic bacteria subjected to freeze-drying. J Appl Microbiol 99:333–338CrossRefGoogle Scholar
  149. Zimmermann K (1987) Einflussparameter und mathematische Modellierung der schonenden Trocknung von Starterkulturen [in German]. Dissertation, Technische Universität MünchenGoogle Scholar
  150. Zotta T, Ricciardi A, Ciocia F, Rossano R, Parente E (2008) Diversity of stress responses in dairy thermophilic streptococci. Int J Food Microbiol 124:34–42CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Chalat Santivarangkna
    • 1
  • Ulrich Kulozik
    • 1
  • Petra Foerst
    • 1
  1. 1.Chair for Food Process Engineering and Dairy Technology, Centre of Life and Food SciencesTechnische Universität MünchenFreising-WeihenstephanGermany

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