Protection mechanisms of sugars during different stages of preparation process of dried lactic acid starter cultures

Food Microbiology

Volumn 25, Issue 3, 2008, Pages 429-441

  Santivarangkna, C ^a   Higl, B ^a   Foerst, P ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Compatible solutes; Glass transition; Lactic acid bacteria; Membrane phase transition; Phospholipid; Sugars; Vitrification

Indexed keywords

CARBOHYDRATE; FOOD PRESERVATIVE; PROBIOTIC AGENT;

BACTERIAL COUNT; DESICCATION; FERMENTATION; FOOD CONTROL; FOOD HANDLING; FOOD PRESERVATION; GROWTH, DEVELOPMENT AND AGING; LACTOBACILLUS; METHODOLOGY; REVIEW;

CARBOHYDRATES; COLONY COUNT, MICROBIAL; DESICCATION; FERMENTATION; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD PRESERVATION; FOOD PRESERVATIVES; FOOD TECHNOLOGY; LACTOBACILLUS; PROBIOTICS;

BACTERIA (MICROORGANISMS);

EID: 40849146891     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2007.12.004     Document Type: Review

References (139)

1. Adams G.D., and Ramsay J.R. Optimizing the lyophilization cycle and the consequences of collapse on the pharmaceutical acceptability of Erwinia l-asparaginase. J. Pharm. Sci. 85 (1996) 1301-1305
2. Aguilera J.M., and Karel M. Preservation of biological materials under desiccation. Crit. Rev. Food Sci. Nutr. 37 (1997) 287-309
3. Ajouz B., Berrier C., Garrigues A., Besnard M., and Ghazi A. Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J. Biol. Chem. 273 (1998) 26670-26674
4. Andersen A.B., Fog-Peterson M.S., Larsen H., and Skibsted L.H. Storage stability of freeze-dried starter cultures (Streptococcus thermophilus) as related to physical state of freezing matrix. Food Sci. Technol. 32 (1999) 540-547
5. Baumann D.P., and Reinbold G.W. Freezing of lactic cultures. J. Dairy Sci. 49 (1966) 259-264
6. Billi D., and Potts M. Life and death of dried prokaryotes. Res. Microbiol. 153 (2002) 7-12
7. Borst J.W., Visser N.V., Kouptsova O., and Visser A.J. Oxidation of unsaturated phospholipids in membrane bilayer mixtures is accompanied by membrane fluidity changes. Biochim. Biophys. Acta 1487 (2000) 61-73
8. Brennan M., Wanismail B., Johnson M.C., and Ray B. Cellular-damage in dried Lactobacillus acidophilus. J. Food Prot. 49 (1986) 47-53
9. Brown A.D. Microbial water stress. Bacteriol. Rev. 40 (1976) 803-846
10. Bryant G., and Wolfe J. Interfacial forces in cryobiology and anhydrobiology. Cryo Lett. 13 (1992) 23-36
11. Bryant G., Koster K.L., and Wolfe J. Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Sci. Res. 11 (2001) 17-25
12. Buera M.P., Rossi S., Moreno S., and Chirife J. DSC confirmation that vitrification is not necessary for stabilization of the restriction enzyme EcoRI dried with saccharides. Biotechnol. Prog. 15 (1999) 577-579
13. Buitink J., van den Dries I.J., Hoekstra F.A., Alberda M., and Hemminga M.A. High critical temperature above T-g may contribute to the stability of biological systems. Biophys. J. 79 (2000) 1119-1128
14. Cacela C., and Hincha D.K. Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes. Biophys. J. 90 (2006) 2831-2842
15. Cacela C., and Hincha D.K. Monosaccharide composition, chain length and linkage type influence the interactions of oligosaccharides with dry phosphatidylcholine membranes. Biochim. Biophys. Acta 1758 (2006) 680-691
16. Carcoba R., and Rodriguez A. 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 (2000) 433-437
17. Carpenter J.F., and Crowe J.H. The mechanism of cryoprotection of proteins by solutes. Cryobiology 25 (1988) 244-255
18. Carpenter J.F., Crowe J.H., and Arakawa T. Comparison of solute-induced protein stabilization in aqueous solution and in the frozen and dried states. J. Dairy Sci. 73 (1990) 3627-3636
19. Carvalho A.S., Silva J., Ho P., Teixeira P., Malcata F.X., and Gibbs P. Survival of freeze-dried Lactobacillus plantarum and Lactobacillus rhamnosus during storage in the presence of protectants. Biotechnol. Lett. 24 (2002) 1587-1591
20. Carvalho A.S., Silva J., Ho P., Teixeira P., Malcata F.X., and Gibbs P. Effect of various growth media upon survival during storage of freeze-dried Enterococcus faecalis and Enterococcus durans. J. Appl. Microbiol. 94 (2003) 947-952
21. Carvalho A.S., Silva J., Ho P., Teixeira P., Malcata F.X., and Gibbs P. 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 (2003) 2538-2541
22. Carvalho A.S., Silva J., Ho P., Teixeira P., Malcata F.X., and Gibbs P. Protective effect of sorbitol and monosodium glutamate during storage of freeze-dried lactic acid bacteria. Lait 83 (2003) 203-210
23. Carvalho A.S., Silva J., Ho P., Teixeira P., Malcata F.X., and Gibbs P. Effects of various sugars added to growth and drying media upon thermotolerance and survival throughout storage of freeze-dried Lactobacillus delbrueckii ssp. bulgaricus. Biotechnol. Prog. 20 (2004) 248-254
24. Castro H.P., Teixeira P., and Kirby R. Storage of lyophilized cultures of Lactobacillus bulgaricus under different relative humidities and atmospheres. Appl. Microbiol. Biotechnol. 44 (1995) 172-176
25. Castro H.P., Teixeira P.M., and Kirby R. Changes in the cell membrane of Lactobacillus bulgaricus during storage following freeze-drying. Biotechnol. Lett. 18 (1996) 99-104
26. Cerning J. Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiol. Rev. 7 (1990) 113-130
27. Chapman D., Williams R.M., and Ladbrooke B.D. Physical studies of phospholipids VI thermotropic and lyotropic mesomorphism of some 1,2-diacyl-phophatidylcholines (lecithins). Chem. Phys. Lipids 1 (1967) 445-475
28. Chavarri F.J., De Paz M., and Nunez M. Cryoprotective agents for frozen concentrated starters from non-bitter Streptococcus lactis strains. Biotechnol. Lett. 10 (1988) 11-16
29. Conrad P.B., Miller D.P., Cielenski P.R., and de Pablo J.J. Stabilization and preservation of Lactobacillus acidophilus in saccharide matrices. Cryobiology 41 (2000) 17-24
30. Cox C.S. Roles of water molecules in bacteria and viruses. Orig. Life Evol. Biosph. 23 (1993) 29-36
31. Crowe J.H., Crowe L.M., and Mouradian R. Stabilization of biological membranes at low water activities. Cryobiology 20 (1983) 346-356
32. Crowe J.H., Crowe L.M., and Chapman D. Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch. Biochem. Biophys. 232 (1984) 400-407
33. Crowe J.H., Crowe L.M., and Hoekstra F.A. Phase transitions and permeability changes in dry membranes during rehydration. J. Bioenerg. Biomembr. 21 (1989) 77-91
34. Crowe J.H., Carpenter J.F., Crowe L.M., and Anchordoguy T.J. Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules. Cryobiology 27 (1990) 219-231
35. Crowe J.H., Hoekstra F.A., Nguyen K.H.N., and Crowe L.M. Is vitrification involved in depression of the phase transition temperature in dry phospholipids?. Biochim. Biophys. Acta-Biomembr. 1280 (1996) 187-196
36. De Antoni G.L., Perez P., Abraham A., and Anon. Trehalose, a cryoprotectant for Lactobacillus bulgaricus. Cryobiology 26 (1989) 149-153
37. Demel R.A., Dorrepaal E., Ebskamp M.J., Smeekens J.C., and De K.B. Fructans interact strongly with model membranes. Biochim. Biophys. Acta 1375 (1998) 36-42
38. Di C.R., De A.M., Limitone A., Minervini F., Carnevali P., Corsetti A., Gaenzle M., Ciati R., and Gobbetti M. Glucan and fructan production by sourdough Weissella cibaria and Lactobacillus plantarum. J. Agric. Food Chem. 54 (2006) 9873-9881
39. Diaz S., Amalfa F., de Lopez B., and Disalvo E.A. Effect of water polarized at the carbonyl groups of phosphatidylcholines on the dipole potential of lipid bilayers. Langmuir 15 (1999) 5179-5182
40. Efiuvwevwere B.J.O., Gorris L.G.M., Smid E.J., and Kets E.P.W. Mannitol-enhanced survival of Lactococcus lactis subjected to drying. Appl. Microbiol. Biotechnol. 51 (1999) 100-104
41. Faraji H., and Lindsay R.C. Characterization of the antioxidant activity of sugars and polyhydric alcohols in fish oil emulsions. J. Agric. Food Chem. 52 (2004) 7164-7171
42. Faraji H., and Lindsay R.C. Antioxidant protection of bulk fish oils by dispersed sugars and polyhydric alcohols. J. Agric. Food Chem. 53 (2005) 736-744
43. Ferreira V., Soares V., Santos C., Silva J., Gibbs P., and Teixeira P. Survival of Lactobacillus sakei during heating, drying and storage in the dried state when growth has occurred in the presence of sucrose or monosodium glutamate. Biotechnol. Lett. 27 (2005) 249-252
44. Fonseca F., Passot S., Cunin O., and Marin M. Collapse temperature of freeze-dried Lactobacillus bulgaricus suspensions and protective media. Biotechnol. Prog. 20 (2004) 229-238
45. Fonseca F., Passot S., Lieben P., and Marin M. Collapse temperature of bacterial suspensions: the effect of cell type and concentration. Cryo Lett. 25 (2004) 425-434
46. Franks F. Freeze-drying of bioproducts: putting principles into practice. Eur. J. Pharm. Biopharm. 45 (1998) 221-229
47. Gancel F., and Novel G. Exopolysaccharide production by Streptococcus salivarius ssp. therrmophilus cultures. 1. Conditions of production. J. Dairy Sci. 77 (1994) 685-688
48. Gillbe C.E., Sage F.J., and Gutteridge J.M.C. Mannitol: molecule magnifique or a case of radical misinterpretation. Free Radic. Res. 24 (1996) 1-7
49. Gilliland S.E. Concentrated starter cultures. In: Gilliland S.E. (Ed). Bacterial Starter Cultures for Foods (1985), CRC Press, Inc., Boca Raton, FL 145-157
50. Glaasker E., Konings W.N., and Poolman B. Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J. Bacteriol. 178 (1996) 575-582
51. Glaasker E., Tjan F.S.B., Ter Steeg P.F., Konings W.N., and Poolman B. Physiological response of Lactobacillus plantarum to salt and nonelectrolyte stress. J. Bacteriol. 180 (1998) 4718-4723
52. Green J.L., and Angell C.A. Phase-relations and vitrification in saccharide-water solutions and the trehalose anomaly. J. Phys. Chem. 93 (1989) 2880-2882
53. Hansen E.B. Commercial bacterial starter cultures for fermented foods of the future. Int. J. Food Microbiol. 78 (2002) 119-131
54. Heckly R.J. Preservation of bacteria by lyophilization. Adv. Appl. Microbiol. 3 (1961) 1-76
55. Higl B., Kurtmann L., Carlsen C.U., Ratjen J., Forst P., Skibsted L.H., Kulozik U., and Risbo J. 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 (2007) 794-800
56. Hoekstra F.A., Golovina E.A., and Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 6 (2001) 431-438
57. Hofvendahl K., and Hahn-Hagerdal B. Factors affecting the fermentative lactic acid production from renewable resources (1). Enzyme Microb. Technol. 26 (2000) 87-107
58. Hutkins R.W. Microbiology and Technology of Fermented Foods (2006), Blackwell Publishing Ltd., Oxford
59. Hutkins R.W., Ellefson W.L., and Kashket E.R. Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus. Appl. Environ. Microbiol. 53 (1987) 2275-2281
60. Imagi J., Yamanouchi T., Okada K., Tanimoto M., and Matsuno R. Properties of agents that effectively entrap liquid lipids. Biosci. Biotechnol. Biochem. 56 (1992) 477-480
61. In 't Veld G., Driessen A.J.M., and Konings W.N. Effect of the unsaturation of phospholipid acyl chains on leucine transport of Lactococcus lactis and membrane permeability. Biochim. Biophys. Acta 1108 (1992) 31-39
62. Izutsu K., and Kojima S. Excipient crystallinity and its protein-structure-stabilizing effect during freeze-drying. J. Pharm. Pharmacol. 54 (2002) 1033-1039
63. Izutsu K., Yoshioka S., and Terao T. Effect of mannitol crystallinity on the stabilization of enzymes during freeze-drying. Chem. Pharm. Bull. (Tokyo) 42 (1994) 5-8
64. Jewell J.B., and Kashket E.R. Osmotically regulated transport of proline by Lactobacillus acidophilus IFO 3532. Appl. Environ. Microbiol. 57 (1991) 2829-2833
65. Joslyn M.A., and Supplee H. Solubility of oxygen in solutions of various sugars. Food Res. 14 (1949) 209-215
66. Kawai K., and Suzuki T. Stabilizing effect of four types of disaccharide on the enzymatic activity of freeze-dried lactate dehydrogenase: step by step evaluation from freezing to storage. Pharm. Res. 24 (2007) 1883-1890
67. Kawai K., Hagiwara T., Takai R., and Suzuki T. Maillard reaction rate in various glassy matrices. Biosci. Biotechnol. Biochem. 68 (2004) 2285-2288
68. Kets E.P.W., and de Bont J.A.M. Protective effect of betaine on survival of Lactobacillus plantarum subjected to drying. FEMS Microbiol. Lett. 116 (1994) 251-255
69. Kets E.P.W., Teunissen P.J.M., and de Bont J.A.M. Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Appl. Environ. Microbiol. 62 (1996) 259-261
70. Kets E.P.W., Groot M.N., Galinski E.A., and de Bont J.A.M. Choline and acetylcholine: novel cationic osmolytes in Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 48 (1997) 94-98
71. Kilimann K.V., Doster W., Vogel R.F., Hartmann C., and Ganzle M.G. Protection by sucrose against heat-induced lethal and sublethal injury of Lactococcus lactis: an FT-IR study. Biochim. Biophys. Acta 1764 (2006) 1188-1197
72. Kim A.I., Akers M.J., and Nail S.L. The physical state of mannitol after freeze-drying: effects of mannitol concentration, freezing rate, and a noncrystallizing cosolute. J. Pharm. Sci. 87 (1998) 931-935
73. Koster K.L., Webb M.S., Bryant G., and Lynch D.V. Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration-vitrification of sugars alters the phase behavior of the phospholipid. Biochim. Biophys. Acta-Biomembr. 1193 (1994) 143-150
74. Koster K.L., Lei Y.P., Anderson M., Martin S., and Bryant G. Effects of vitrified and nonvitrified sugars on phosphatidylcholine fluid-to-gel phase transitions. Biophys. J. 78 (2000) 1932-1946
75. Koster K.L., Maddocks K.J., and Bryant G. Exclusion of maltodextrins from phosphatidylcholine multilayers during dehydration: effects on membrane phase behaviour. Eur. Biophys. J. 32 (2003) 96-105
76. Laroche C., and Gervais P. Unexpected thermal destruction of dried, glass bead-immobilized microorganisms as a function of water activity. Appl. Environ. Microbiol. 69 (2003) 3015-3019
77. Laroche C., Fine F., and Gervais P. Water activity affects heat resistance of microorganisms in food powders. Int. J. Food Microbiol. 97 (2005) 307-315
78. Le M.C., Bon E., and Lonvaud-Funel A. Tolerance to high osmolality of the lactic acid bacterium Oenococcus oeni and identification of potential osmoprotectants. Int. J. Food Microbiol. 115 (2007) 335-342
79. Lee C.W., Waugh J.S., and Griffin R.G. Solid-state NMR study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry 25 (1986) 3737-3742
80. Lenne T., Bryant G., Holcomb R., and Koster K.L. How much solute is needed to inhibit the fluid to gel membrane phase transition at low hydration?. Biochim. Biophys. Acta 1768 (2007) 1019-1022
81. Leslie S.B., Teter S.A., Crowe L.M., and Crowe J.H. Trehalose lowers membrane phase transitions in dry yeast cells. Biochim. Biophys. Acta-Biomembr. 1192 (1994) 7-13
82. Leslie S.B., Israeli E., Lighthart B., Crowe J.H., and Crowe L.M. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl. Environ. Microbiol. 61 (1995) 3592-3597
83. Lievense L.C., and van 't Riet K. Convective drying of bacteria. II. Factors influencing survival. Adv. Biochem. Eng. Biotechnol. 51 (1994) 71-89
84. Linders J.M., de Jong G.I.W., Meerdink G., and Vantriet K. Carbohydrates and the dehydration inactivation of Lactobacillus plantarum: the role of moisture distribution and water activity. J. Food Eng. 31 (1997) 237-250
85. Linders L.J.M., Meerdink G., and Vantriet K. Effect of growth parameters on the residual activity of Lactobacillus plantarum after drying. J. Appl. Microbiol. 82 (1997) 683-688
86. Linders L.J.M., Wolkers W.F., Hoekstra F.A., and Vantriet K. Effect of added carbohydrates on membrane phase behavior and survival of dried Lactobacillus plantarum. Cryobiology 35 (1997) 31-40
87. Lodato P., de Huergo M.S., and Buera M.P. Viability and thermal stability of a strain of Saccharomyces cerevisiae freeze-dried in different sugar and polymer matrices. Appl. Microbiol. Biotechnol. 52 (1999) 215-220
88. Luzardo M.C., Amalfa F., Nunez A.M., Diaz S., de Lopez A.C.B., and Disalvo E.A. Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys. J. 78 (2000) 2452-2458
89. Mattick K.L., Jorgensen F., Legan J.D., Lappin-Scott H.M., and Humphrey T.J. Habituation of Salmonella spp. at reduced water activity and its effect on heat tolerance. Appl. Environ. Microbiol. 66 (2000) 4921-4925
90. Mattick K.L., Jorgensen F., Wang P., Pound J., Vandeven M.H., Ward L.R., Legan J.D., Lappin-Scott H.M., and Humphrey T.J. Effect of challenge temperature and solute type on heat tolerance of Salmonella serovars at low water activity. Appl. Environ. Microbiol. 67 (2001) 4128-4136
91. Mazur P. Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247 (1984) C125-C142
92. Mazur P., Leibo S.P., and Chu E.H.Y. 2-Factor hypothesis of freezing injury-evidence from chinese-hamster tissue culture cells. Exp. Cell Res. 71 (1972) 345-355
93. Mille Y., Obert J.P., Beney L., and Gervais P. New drying process for lactic bacteria based on their dehydration behavior in liquid medium. Biotechnol. Bioeng. 88 (2004) 71-76
94. Miller D.P., Anderson R.E., and de Pablo J.J. Stabilization of lactate dehydrogenase following freeze thawing and vacuum-drying in the presence of trehalose and borate. Pharm. Res. 15 (1998) 1215-1221
95. Miyamoto-Shinohara Y., Imaizumi T., Sukenobe J., Murakami Y., Kawamura S., and Komatsu Y. Survival rate of microbes after freeze-drying and long term storage. Cryobiology 41 (2000) 251-255
96. Mozzi F., Rollan G., de Giori G.S., and de Valdez F. Effect of galactose and glucose on the exopolysaccharide production and the activities of biosynthetic enzymes in Lactobacillus casei CRL 87. J. Appl. Microbiol. 91 (2001) 160-167
97. Obis D., Guillot A., and Mistou M.Y. 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 (2001) 39-44
98. Ohtake S., Schebor C., Palecek S.P., and de Pablo J.J. Effect of pH, counter ion, and phosphate concentration on the glass transition temperature of freeze-dried sugar-phosphate mixtures. Pharm. Res. 21 (2004) 1615-1621
99. Oldenhof H., Wolkers W.F., Fonseca F., Passot S.P., and Marin M. Effect of sucrose and maltodextrin on the physical properties and survival of air-dried Lactobacillus bulgaricus: an in situ Fourier transform infrared spectroscopy study. Biotechnol. Prog. 21 (2005) 885-892
100. Panoff J.M., Thammavongs B., and Gueguen M. Cryoprotectants lead to phenotypic adaptation to freeze-thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40 (2000) 264-269
101. Pereira C.S., and Hunenberger P.H. Interaction of the sugars trehalose, maltose and glucose with a phospholipid bilayer: a comparative molecular dynamics study. J. Phys. Chem. B, Condens. Matter Mater. Surf. Interfaces Biophys. 110 (2006) 15572-15581
102. Pereira C.S., Lins R.D., Chandrasekhar I., Freitas L.C., and Hunenberger P.H. Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study. Biophys. J. 86 (2004) 2273-2285
103. Poolman B., and Glaasker E. Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 29 (1998) 397-407
104. Potts M. Desiccation tolerance of prokaryotes. Microbiol. Rev. 58 (1994) 755-805
105. Potts M. Desiccation tolerance: a simple process?. Trends Microbiol. 9 (2001) 553-559
106. Roberson E.B., and Firestone M.K. Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl. Environ. Microbiol. 58 (1992) 1284-1291
107. Roberts I.S. The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu. Rev. Microbiol. 50 (1996) 285-315
108. Roos Y.H. Melting and glass transitions of low molecular weight carbohydrates. Carbohydr. Res. 238 (1993) 39-48
109. Sagone Jr. A.L., Greenwald J., Kraut E.H., Bianchine J., and Singh D. Glucose: a role as a free radical scavenger in biological systems. J. Lab Clin. Med. 101 (1983) 97-104
110. Santivarangkna C., Kulozik U., and Foerst P. Effect of carbohydrates on the survival of Lactobacillus helveticus during vacuum drying. Lett. Appl. Microbiol. 42 (2006) 271-276
111. Santivarangkna C., Wenning M., Foerst P., and Kulozik U. Damage of cell envelope of Lactobacillus helveticus during vacuum drying. J. Appl. Microbiol. 102 (2007) 748-756
112. Santos H., and da Costa M.S. Compatible solutes of organisms that live in hot saline environments. Environ. Microbiol. 4 (2002) 501-509
113. Schebor C., Galvagno M., Buera M.D., and Chirife J. Glass transition temperatures and fermentative activity of heat-treated commercial active dry yeasts. Biotechnol. Prog. 16 (2000) 163-168
114. Schwab C., Vogel R., and Ganzle M.G. Influence of oligosaccharides on the viability and membrane properties of Lactobacillus reuteri TMW1.106 during freeze-drying. Cryobiology 55 (2007) 108-114
115. Selmer-Olsen E., Birkeland S.E., and Sorhaug T. Effect of protective solutes on leakage from and survival of immobilized Lactobacillus subjected to drying, storage and rehydration. J. Appl. Microbiol. 87 (1999) 429-437
116. Silva J., Carvalho A.S., Pereira H., Teixeira P., and Gibbs P.A. Induction of stress tolerance in Lactobacillus delbrueckii ssp. bulgaricus by the addition of sucrose to the growth medium. J. Dairy Res. 71 (2004) 121-125
117. Sum A.K., Faller R., and de Pablo J.J. Molecular simulation study of phospholipid bilayers and insights of the interactions with disaccharides. Biophys. J. 85 (2003) 2830-2844
118. Tamaru Y., Takani Y., Yoshida T., and Sakamoto T. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol. 71 (2005) 7327-7333
119. Teixeira P., Castro H., and Kirby R. Spray drying as a method for preparing concentrated cultures of Lactobacillus bulgaricus. J. Appl. Bacteriol. 78 (1995) 456-462
120. To B.C.S., and Etzel M.R. Spray drying, freeze drying, or freezing of three different lactic acid bacteria species. J. Food Sci. 62 (1997) 576-585
121. Torino M.I., Hebert E.M., Mozzi F., and de Valdez F. Growth and exopolysaccharide production by Lactobacillus helveticus ATCC 15807 in an adenine-supplemented chemically defined medium. J. Appl. Microbiol. 99 (2005) 1123-1129
122. Tsvetkov T., and Brankova R. Viability of micrococci and lactobacilli upon freezing and freeze drying in the presence of different cryoprotectants. Cryobiology 20 (1983) 318-323
123. Tymczyszyn E.E., Gomez-Zavaglia A., and Disalvo E.A. Effect of sugars and growth media on the dehydration of Lactobacillus delbrueckii ssp. bulgaricus. J. Appl. Microbiol. 102 (2007) 845-851
124. Vereyken I.J., Chupin V., Demel R.A., Smeekens S.C., and de Kruijff B. Fructans insert between the headgroups of phospholipids. Biochim. Biophys. Acta 1510 (2001) 307-320
125. Vereyken I.J., Chupin V., Hoekstra F.A., Smeekens S.C., and de Kruijff B. The effect of fructan on membrane lipid organization and dynamics in the dry state. Biophys. J. 84 (2003) 3759-3766
126. Vereyken I.J., van Kuik J.A., Evers T.H., Rijken P.J., and de Kruijff B. Structural requirements of the fructan-lipid interaction. Biophys. J. 84 (2003) 3147-3154
127. Villarreal M.A., Diaz S.B., Disalvo E.A., and Montich G.G. Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir 20 (2004) 7844-7851
128. Wang W. Lyophilization and development of solid protein pharmaceuticals. Int. J. Pharm. 203 (2000) 1-60
129. Wang Y.C., Yu R.C., and Chou C.C. Viability of lactic acid bacteria and bifidobacteria in fermented soymilk after drying, subsequent rehydration and storage. Int. J. Food Microbiol. 93 (2004) 209-217
130. Ward K.R., Adams G.D., Alpar H.O., and Irwin W.J. Protection of the enzyme l-asparaginase during lyophilisation-a molecular modelling approach to predict required level of lyoprotectant. Int. J. Pharm. 187 (1999) 153-162
131. Wehmeier K.R., and Mooradian A.D. Autoxidative and antioxidative potential of simple carbohydrates. Free Radic. Biol. Med. 17 (1994) 83-86
132. Welsh D.T., and Herbert R.A. Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. FEMS Microbiol. Lett. 174 (1999) 57-63
133. Wiener M.C., Suter R.M., and Nagle J.F. Structure of the fully hydrated gel phase of dipalmitoylphosphatidylcholine. Biophys. J. 55 (1989) 315-325
134. Wisselink H.W., Weusthuis R.A., Eggink G., Hugenholtz J., and Grobben G.J. Mannitol production by lactic acid bacteria: a review. Int. Dairy J. 12 (2002) 151-161
135. Wolfe J. Lateral stresses in membranes at low water potential. Aus. J. Plant Physiol. 14 (1987) 311-318
136. Wolfe J., and Bryant G. Freezing, drying, and/or vitrification of membrane-solute-water systems. Cryobiology 39 (1999) 103-129
137. Yancey P.H. Water stress, osmolytes and proteins. Am. Zool. 41 (2001) 699-709
138. Zaunmuller T., Eichert M., Richter H., and Unden G. Variations in the energy metabolism of biotechnologically relevant heterofermentative lactic acid bacteria during growth on sugars and organic acids. Appl. Microbiol. Biotechnol. 72 (2006) 421-429
139. Zhao G., and Zhang G. Effect of protective agents, freezing temperature, rehydration media on viability of malolactic bacteria subjected to freeze-drying. J. Appl. Microbiol. 99 (2005) 333-338