Control of cell morphology of probiotic Lactobacillus acidophilus for enhanced cell stability during industrial processing

International Journal of Food Microbiology

Volumn 192, Issue , 2015, Pages 34-42

  Senz, Martin ^a,b   van Lengerich, Bernhard ^c   Bader, Johannes ^d   Stahl, Ulf ^a,b  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b Institute for Microbiology Immunology and Laboratory Medicine   (Germany)

^c GENERAL MILLS INC   (United States)

^d BEUTH UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Cell stability; Extrusion encapsulation; Lactobacillus acidophilus NCFM; Maillard reaction products; Medium composition; Morphology

Indexed keywords

CASEIN; GLUCOSE; PEPTONE; PROBIOTIC AGENT; CULTURE MEDIUM;

ADAPTATION; ARTICLE; BACTERIAL CELL; BACTERIAL VIABILITY; CELL COUNT; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CELL VOLUME; CULTURE MEDIUM; DAIRY INDUSTRY; ENCAPSULATION; FREEZE DRYING; HEATING; LACTOBACILLUS ACIDOPHILUS; NONHUMAN; PROCESSING; SHELF LIFE; STARTER CULTURE; STORAGE; STORAGE TEMPERATURE; THERMAL EXPOSURE; THERMODYNAMICS; CELL SURVIVAL; CYTOLOGY; FOOD HANDLING; PHYSIOLOGY;

LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS ACIDOPHILUS NCFM;

CELL SHAPE; CELL SURVIVAL; CULTURE MEDIA; FOOD HANDLING; LACTOBACILLUS ACIDOPHILUS; PROBIOTICS;

EID: 84907993354     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.09.015     Document Type: Article

References (56)

1. Abadias M., Teixido N., Usall J., Benabarre A., Vinas I. Viability, efficacy, and storage stability of freeze-dried biocontrol agent Candida sake using different protective and rehydration media. J. Food Prot. 2001, 64:856-861.
2. Achour M., Mtimet N., Cornelius C., Zgouli S., Mahjoub A., Thonart P., Hamdi M. Application of the accelerated shelf life testing method ASLT to study the survival rates of freeze-dried Lactococcus starter cultures. J. Chem. Technol. Biotechnol. 2001, 76:624-628.
3. Altermann E., Buck L.B., Cano R., Klaenhammer T.R. Identification and phenotypic characterization of the cell-division protein CdpA. Gene 2004, 342:189-197.
4. Ananta E., Birkeland S.E., Corcoran B., Fitzgerald G., Hinz S., Klijn A., Mättö J., Mercernier A., Nilsson U., Nyman M., O'Sullivan E., Parche S., Rautonen N., Ross R.P., Saarela M., Stanton C., Stahl U., Suomalainen T., Vincken J.P., Virkajärvi I., Voragen F., Wesenfeld J., Wouters R., Knorr D. Processing effects on the nutritional advancement of probiotics and prebiotics. Microb. Ecol. Health Dis. 2004, 16(2-3):113-124.
5. BD Biopharmaceutical Production, Bionutrient Technical Manuel 2004, (7). Second edition.
6. Beck W.S., Levin M. Purification, kinetics, and repression control of bacterial trans-N-deoxyribosylase. J. Biol. Chem. 1963, 238:702-709.
7. Castro H.P., Teixeira P.M., Kirby R. Storage of lyophilized cultures of Lactobacillus bulgaricus under different relative humidities and atmospheres. Appl. Microbiol. Biotechnol. 1995, 44:172-176.
8. Chawdhri R.F., Hutchinson D.W., Richards A.O.L. Nucleoside deoxyribosyltransferase and inosine phosphorylase activity in lactic acid bacteria. Arch. Microbiol. 1991, 155:409-411.
9. De Man J.D., Rogosa M., Sharpe M.E. A medium for the cultivation of lactobacilli. J. Appl. Bacteriol. 1960, 23:130-135.
10. Deepika G., Green R.J., Frazier R.A., Charalampopoulos D. Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J. Appl. Microbiol. 2009, 107:1230-1240.
11. Deibel R.H., Downing M., Niven C.F., Schweigert B.S. Filament formation by Lactobacillus leichmannii when desoxyribosides replace vitamin B12 in the growth medium. J. Bacteriol. 1956, 71:255-256.
12. EFSA EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA). Scientific opinion on the substantiation of health claims related to non-characterised bacteria and yeasts pursuant to article 13(1) of regulation (EC) No. 1924/2006. EFSA J. 2010, 8(2):1470. (44).
13. Einarsson H., Snygg B.G., Eriksson C. Inhibition of bacterial growth by Maillard reaction products. J. Agric. Food Chem. 1983, 31:1043-1047.
14. FAO/WHO 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 2002, 1-11.
15. Fonseca F., Beal C., Corrieu G. Method of quantifying the loss of acidification activity of lactic acid starters during freezing and frozen storage. J. Dairy Res. 2000, 67:83-90.
16. Gardiner G.E., O'Sullivan E., Kelly J., Auty M.A., Fitzgerald G.F., Collins J.K. Comparative survival rates of human-derived probiotic Lactobacillus paracasei and L. salivarius strains during heat treatment and spray-drying. Appl. Environ. Microbiol. 2000, 66:2605-2612.
17. Greenspan L. Humidity fixed points of binary saturated aqueous solutions. J. Res. Natl. Bur. Stand. 1977, 81:89-96.
18. Grzeskowiak L., Isolauri E., Salminen S., Gueimonde M. Manufacturing process influences properties of probiotic bacteria. Br. J. Nutr. 2010, 105(6):887-894.
19. Helou C., Marier D., Jacolot P., Abdennebi-Najar L., Niquet-Léridon C., Tessier F., Gadonna-Widehem P. Microorganisms and Maillard reaction products: a review of the literature and recent findings. Amino Acids 2014, 46:267-277.
20. Hiramoto K., Kido K., Kikugawa K. DNA breaking by Maillard products of glucose-amino acid mixtures formed in an aqueous system. J. Agric. Food Chem. 1994, 42:689-694.
21. Ives D.H., Ikeda S. Life on the salvage path: the deoxynucleoside kinase of Lactobacillus acidophilus R-26. Prog. Nucleic Acid Res. Mol. Biol. 1998, 59:205-255.
22. Jeener H., Jeener R. Cytochemical observations on Thermobacterium acidophilus R26 after inhibition of growth by desoxyribonucleosides or uracil. Arch. Int. Physiol. Biochim. Biophys. 1952, 60:194-195.
23. Justice S.S., Hunstad D.A., Cegelski L., Hultgren S.J. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 2008, 6:162-168.
24. Kilstrup M., Hammer K., Ruhdal Jensen P., Martinussen J. Nucleotide metabolism and its control in lactic acid bacteria. FEMS Microbiol. Rev. 2005, 29:555-590.
25. King V.A., Lin H.J., Liu C.F. Accelerated storage testing of freeze-dried and controlled low-temperature vacuum dehydrated Lactobacillus acidophilus. J. Gen. Appl. Microbiol. 1998, 44:160-165.
26. Kojima M., Suda S., Hotta S., Hamada K. Induction of pleomorphy and calcium ion deficiency in Lactobacillus bifidus. J. Bacteriol. 1970, 102:217-220.
27. Kusaka I., Kitahara K. Effect of several vitamins on the cell division and the growth of Lactobacillus delbrueckii. J. Vitaminol. (Kyoto) 1962, 8:115-120.
28. Mattarelli P., Biavati B., Pesenti M., Crociani F. Effect of growth temperature on the biosynthesis of cell wall proteins from Bifidobacterium globosum. Res. Microbiol. 1999, 150:117-127.
29. Mattila-Sandholm T., Mättö J., Saarela M. Lactic acid bacteria with health claims-interactions and interference with gastrointestinal flora. Int. Dairy J. 1999, 9:25-35.
30. Millsap K.W., van der Mei H.C., Reid G., Busscher H.J. Physico-chemical and adhesive cell surface properties of Lactobacillus strains grown in old formula and new, standardized MRS medium. J. Microbiol. Methods 1996, 27:239-242.
31. Morales F.J., Jiménez-Pérez S. Free radical scavenging capacity of Maillard reaction products as related to colour and fluorescence. Food Chem. 2001, 72:119-125.
32. Mulvey M.A., Lopez-Boado Y.S., Wilson C.L., Roth R., Parks W.C., Heuser J., Hultgren S.J. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998, 282:1494-1497.
33. Popov I.N., Lewin G. Photochemiluminescent detection of antiradical activity: II. Testing of nonenzymic water-soluble antioxidants. Free Radic. Biol. Med. 1994, 17:267-271.
34. Ramsey H.H., Lankford C.E. Stimulation of growth initiation by heat degradation products of glucose. J. Bacteriol. 1956, 72:511-518.
35. Rechinger K.B., Siegumfeldt H., Svendsen I., Jakobsen M. "Early" protein synthesis of Lactobacillus delbrueckii ssp. bulgaricus in milk revealed by (35S) methionine labeling and two-dimensional gel electrophoresis. Electrophoresis 2000, 21:2660-2669.
36. Reich J., Soska J. Thymineless death in Lactobacillus acidophilus R-26 II. Factors determining the rate of the reproductive inactivation. Folia Microbiol. (Praha) 1973, 18:361-367.
37. Rhee S.K., Pack M.Y. Effect of environmental pH on chain length of Lactobacillus bulgaricus. J. Bacteriol. 1980, 144:865-868.
38. Rogers D., King T.E., Cheldelin V.H. Growth stimulation of Lactobacillus gayoni by N-d-glucosylglycine. Proc. Soc. Exp. Biol. Med. 1953, 82:140-144.
39. Saarela M., Rantala M., Hallamaa K., Nohynek L., Virkajarvi I., Matto J. Stationary-phase acid and heat treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. J. Appl. Microbiol. 2004, 96:1205-1214.
40. Santivarangkna C., Kulozik U., Foerst P. Alternative drying processes for the industrial preservation of lactic acid starter cultures. Biotechnol. Prog. 2007, 23:302-315.
41. Schar-Zammaretti P., Dillmann M.L., D'Amico N., Affolter M., Ubbink J. Influence of fermentation medium composition on physicochemical surface properties of Lactobacillus acidophilus. Appl. Environ. Microbiol. 2005, 71:8165-8173.
42. Talwalkar A., Kailasapathy K. The role of oxygen in the viability of probiotic bacteria with reference to L. acidophilus and Bifidobacterium spp. Curr. Issues Intest. Microbiol. 2004, 5:1-8.
43. Teixeira P., Castro H., Malcata F.X., Kirby R.M. Survival of Lactobacillus delbruekii spp. bulgaricus following spray-drying. J. Dairy Sci. 1995, 78:1025-1031.
44. Teixeira P., Castro H., Kirby R. Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett. Appl. Microbiol. 1996, 22:34-38.
45. Tuomola E., Crittenden R., Playne M., Isolauri E., Salminen S. Quality assurance criteria for probiotic bacteria. Am. J. Clin. Nutr. 2001, 73:393S-398S.
46. Van Lengerich B. Encapsulation of sensitive liquid components into a matrix to obtain discrete shelfstable particle (US7201923B1) 2007.
47. Van Lengerich B., Senz M., Stahl U., Mast-Gerlach E. Means and methods of increasing viability of rod-shaped bacteria (WO2013068585A1) 2011.
48. Wang H.-Y., Qian H., Yao W.-R. Melanoidins produced by the Maillard reaction: structure and biological activity. Food Chem. 2013, 128:573-584.
49. Webb M. The influence of magnesium on cell division: the effect of magnesium on the growth and cell division of various bacterial species in complex media. J. Gen. Microbiol. 1949, 3:410-417.
50. Webb M. The influence of magnesium on cell division: the effect of magnesium on the growth of bacteria in simple chemically defined media. J. Gen. Microbiol. 1949, 3:418-424.
51. Wijewickreme A.N., Kitts D.D. Influence of reaction conditions on the oxidative behavior of model Maillard reaction products. J. Agric. Food Chem. 1997, 45:4571-4576.
52. Wright C.T., Klaenhammer T.R. Calcium-induced alteration of cellular morphology affecting the resistance of Lactobacillus acidophilus to freezing. Appl. Environ. Microbiol. 1981, 41:807-815.
53. Wright C.T., Klaenhammer T.R. Survival of Lactobacillus bulgaricus during freezing and freeze-drying after growth in the presence of calcium. J. Food Sci. 1983, 48:773-777.
54. Wright C.T., Klaenhammer T.R. Influence of calcium and manganese on dechaining of Lactobacillus bulgaricus. Appl. Environ. Microbiol. 1983, 46:785-792.
55. Yilmaz Y., Toledo R. Antioxidant activity of water-soluble Maillard reaction products. Food Chem. 2005, 93:273-278.
56. Zayed G., Roos Y.H. Influence of trehalose and moisture content on survival of Lactobacillus salivarius subjected to freeze-drying and storage. Process Biochem. 2004, 39:1081-1086.