Biochemical engineering approaches for increasing viability and functionality of probiotic bacteria

International Journal of Molecular Sciences

Volumn 17, Issue 6, 2016, Pages

  Nguyen, Huu Thanh ^a,b   Truong, Dieu Hien ^a   Kouhoundé, Sonagnon ^b   Ly, Sokny ^b   Razafindralambo, Hary ^b   Delvigne, Frank ^b  

^a TON DUC THANG UNIVERSITY   (Viet Nam)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Biochemical engineering; Cellular robustness; Exopolysaccharide; Prebiotics; Probiotics; Sub lethal stress; Survival

Indexed keywords

EXOPOLYSACCHARIDE; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

AMPLITUDE MODULATION; BACTERIAL VIABILITY; BIFIDOBACTERIUM BIFIDUM; BIOCHEMICAL ANALYSIS; BIOENGINEERING; BIOSYNTHESIS; DNA DAMAGE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; FOOD INTAKE; HUMAN; MICROBIOLOGY; NONHUMAN; OSMOTIC STRESS; OXIDATION REDUCTION POTENTIAL; PH; PLEIOTROPY; REVIEW; TEMPERATURE; ADAPTATION; BACTERIUM; ENVIRONMENT; FERMENTATION; FOOD CONTROL; GENETICS; METABOLIC ENGINEERING; METABOLISM; MICROBIAL VIABILITY; PHYSIOLOGICAL STRESS; QUANTITATIVE TRAIT;

ADAPTATION, BIOLOGICAL; BACTERIA; ENVIRONMENT; FERMENTATION; FOOD MICROBIOLOGY; METABOLIC ENGINEERING; MICROBIAL VIABILITY; PROBIOTICS; QUANTITATIVE TRAIT, HERITABLE; STRESS, PHYSIOLOGICAL;

EID: 84971656793     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17060867     Document Type: Review

References (128)

1. Roy, D. Technological aspects related to the use of bifidobacteria in dairy products. Lait 2005, 85, 39-56. [CrossRef]
2. Madden, J.A.J, Hunter, J.O. A review of the role of the gut microflora in irritable bowel syndrome and the effects of probiotics. Br. J. Nutr. 2002, 88, s67-s72. [CrossRef] [PubMed]
3. Eutamene, H, Bueno, L. Role of probiotics in correcting abnormalities of colonic flora induced by stress. Gut 2007, 56, 1495-1497. [CrossRef] [PubMed]
4. Balcázar, J.L, Blas, I.D, Ruiz-Zarzuela, I, Cunningham, D, Vendrell, D, Múzquiz, J.L. The role of probiotics in aquaculture. Vet. Microbiol. 2006, 114, 173-186.
5. Foligné, B, Daniel, C, Pot, B. Probiotics from research to market: The possibilities, risks and challenges. Curr. Opin. Microbiol. 2013, 16, 284-292. [CrossRef] [PubMed]
6. Huys, G, Botteldoorn, N, Delvigne, F, de Vuyst, L, Heyndrickx, M, Pot, B, Dubois, J.J, Daube, G. Microbial characterization of probiotics—Advisory report of the working group “8651 probiotics” of the belgian Superior Health Council (SHC). Mol. Nutr. Food Res. 2013, 57, 1479-1504. [CrossRef] [PubMed]
7. Lacroix, C, Yildirim, S. Fermentation technologies for the production of probiotics with high viability and functionality. Curr. Opin. Biotechnol. 2007, 18, 176-183. [CrossRef] [PubMed]
8. Nguyen, H.T, Razafindralambo, H, Blecker, C, N’Yapo, C, Thonart, P, Delvigne, F. Stochastic exposure to sub-lethal high temperature enhances exopolysaccharides (EPS) excretion and improves Bifidobacterium bifidum cell survival to freeze-drying. Biochem. Eng. J. 2014, 88, 85-94. [CrossRef]
9. Matijasic, M, Mestrovic, T, Peric, M, Cipcic Paljetak, H, Panek, M, Vranesic Bender, D, Ljubas Kelecic, D, Krznaric, Z, Verbanac, D. Modulating composition and metabolic activity of the gut microbiota in IBD patients. Int. J. Mol. Sci. 2016, 17. [CrossRef] [PubMed]
10. Bachmann, H, Pronk, J.T, Kleerebezem, M, Teusink, B. Evolutionary engineering to enhance starter culture performance in food fermentations. Curr. Opin. Biotechnol. 2015, 32, 1-7. [CrossRef] [PubMed]
11. Dragosits, M, Mattanovich, D. Adaptive laboratory evolution—Principles and applications for biotechnology. Microb. Cell Fact. 2013, 12, 64. [CrossRef] [PubMed]
12. Volkert, M, Ananta, E, Luscher, C, Knorr, D. Effect of air freezing, spray freezing, and pressure shift freezing on membrane integrity and viability of Lactobacillus rhamnosus gg. J. Food Eng. 2008, 87, 532-540. [CrossRef]
13. Nguyen, H, Razafindralambo, H, Richel, A, Jacquet, N, Evrard, P, Antoine, P, Thonart, P, Delvigne, F. Scalable temperature induced stress for the large-scale production of functionalized bifidobacteria. J. Ind. Microbiol. Biotechnol. 2015, 42, 1225-1231. [CrossRef] [PubMed]
14. Mozzetti, V, Grattepanche, F, Berger, B, Rezzonico, E, Arigoni, F, Lacroix, C. Fast screening of bifidobacterium longum sublethal stress conditions in a novel two-stage continuous culture strategy. Benef. Microb. 2013, 4, 167-178. [CrossRef] [PubMed]
15. Ryall, B, Eydallin, G, Ferenci, T. Culture history and population heterogeneity as determinants of bacterial adaptation: The adaptomics of a single environmental transition. Microbiol. Mol. Biol. Rev. 2012, 76, 597-625. [CrossRef] [PubMed]
16. Abee, T, Wels, M, de Been, M, den Besten, H. From transcriptional landscapes to the identification of biomarkers for robustness. Microb. Cell Fact. 2011, 10, S9. [CrossRef] [PubMed]
17. Mills, S, Stanton, C, Fitzgerald, G.F, Ross, R.P. Enhancing the stress responses of probiotics for a lifestyle from gut to product and back again. Microb. Cell Fact. 2011, 10, S19. [PubMed]
18. Corcoran, B.M, Stanton, C, Fitzgerald, G, Ross, R.P. Life under stress: The probiotic stress response and how it may be manipulated. Curr. Pharm. Des. 2008, 14, 1382-1399. [CrossRef] [PubMed]
19. Ruiz, L, Margolles, A, Sanchez, B. Bile resistance mechanisms in lactobacillus and bifidobacterium. Front. Microbiol. 2013, 4, 396. [CrossRef] [PubMed]
20. Booth, I.R. Stress and the single cell: Intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int. J. Food Microbiol. 2002, 78, 19-30. [CrossRef]
21. Delvigne, F, Zune, Q, Lara, A.R, Al-Soud, W, Sorensen, S.J. Metabolic variability in bioprocessing: Implications of microbial phenotypic heterogeneity. Trends Biotechnol. 2014, 32, 608-616. [CrossRef] [PubMed]
22. Martins, B.M, Locke, J.C. Microbial individuality: How single-cell heterogeneity enables population level strategies. Curr. Opin. Microbiol. 2015, 24, 104-112. [CrossRef] [PubMed]
23. Davey, H.M. Life, death, and in-between: Meanings and methods in microbiology. Appl. Environ. Microbiol. 2011, 77, 5571-5576. [CrossRef] [PubMed]
24. Bridier, A, Hammes, F, Canette, A, Bouchez, T, Briandet, R. Fluorescence-based tools for single-cell approaches in food microbiology. Int. J. Food Microbiol. 2015, 213, 2-16. [CrossRef] [PubMed]
25. Brognaux, A, Han, S, Sorensen, S.J, Lebeau, F, Thonart, P, Delvigne, F. A low-cost, multiplexable, automated flow cytometry procedure for the characterization of microbial stress dynamics in bioreactors. Microb. Cell Fact. 2013, 12, 100. [CrossRef] [PubMed]
26. Delvigne, F, Baert, J, Gofflot, S, Lejeune, A, Telek, S, Johanson, T, Lantz, A.E. Dynamic single-cell analysis of saccharomyces cerevisiae under process perturbation: Comparison of different methods for monitoring the intensity of population heterogeneity. J. Chem. Technol. Biotechnol. 2015, 90, 314-323. [CrossRef]
27. Delvigne, F, Goffin, P. Microbial heterogeneity affects bioprocess robustness: Dynamic single-cell analysis contributes to understanding of microbial populations. Biotechnol. J. 2014, 9, 61-72. [CrossRef] [PubMed]
28. Teusink, B, Bachmann, H, Molenaar, D. Systems biology of lactic acid bacteria: A critical review. Microb. Cell Fact. 2011, 10, S11. [CrossRef] [PubMed]
29. Doleyres, Y, Fliss, I, Lacroix, C. Increased stress tolerance of bifidobacterium longum and Lactococcus lactis produced during continuous mixed-strain immobilized-cell fermentation. J. Appl. Microbiol. 2004, 97, 527-539. [CrossRef] [PubMed]
30. Doleyres, Y, Lacroix, C. Technologies with free and immobilised cells for probiotic bifidobacteria production and protection. Int. Dairy J. 2005, 15, 973-988. [CrossRef]
31. Delvigne, F, Destain, J, Thonart, P. A methodology for the design of scale-down bioreactors by the use of mixing and circulation stochastic models. Biochem. Eng. J. 2006, 28, 256-268. [CrossRef]
32. Delvigne, F, brognaux, A, Gorret, N, Neubauer, P, Delafosse, A, Collignon, M.-L, Toye, D, Crine, M, Boxus, M, Thonart, P. Characterization of the response of GFP microbial biosensors sensitive to substrate limitation in scale-down bioreactors. Biochem. Eng. J. 2011, 55, 131-139. [CrossRef]
33. Delvigne, F, Brognaux, A, Francis, F, Twizere, J.C, Gorret, N, Sorensen, S.J, Thonart, P. Green fluorescent protein (GFP) leakage from microbial biosensors provides useful information for the evaluation of the scale-down effect. Biotechnol. J. 2011, 6, 968-978. [CrossRef] [PubMed]
34. Neubauer, P, Junne, S. Scale-down simulators for metabolic analysis of large-scale bioprocesses. Curr. Opin. Biotechnol. 2010, 21, 114-121. [CrossRef] [PubMed]
35. Schweder, T. Bioprocess monitoring by marker gene analysis. Biotechnol. J. 2011, 6, 926-933. [CrossRef] [PubMed]
36. Desmond, C, Stanton, C, Fitzgerald, G.F, Collins, K, Paul Ross, R. Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int. Dairy J. 2001, 11, 801-808. [CrossRef]
37. Prasad, J, McJarrow, P, Gopal, P. Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl. Environ. Microbiol. 2003, 69, 917-925. [CrossRef] [PubMed]
38. 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. [CrossRef] [PubMed]
39. Serrazanetti, D.I, Guerzoni, M.E, Corsetti, A, Vogel, R. Metabolic impact and potential exploitation of the stress reactions in lactobacilli. Food Microbiol. 2009, 26, 700-711. [CrossRef] [PubMed]
40. Ananta, E, Volkert, M, Knorr, D. Cellular injuries and storage stability of spray-dried Lactobacillus rhamnosus gg. Int. Dairy J. 2005, 15, 399-409. [CrossRef]
41. Abee, T, Wouters, J.A. Microbial stress response in minimal processing. Int. J. Food Microbiol. 1999, 50, 65-91. [CrossRef]
42. De Angelis, M, Gobbetti, M. Environmental stress responses in lactobacillus: A review. Proteomics 2004, 4, 106-122. [CrossRef] [PubMed]
43. Kim, W.S, Perl, L, Park, J.H, Tandianus, J.E, Dunn, N.W. Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr. Microbiol. 2001, 43, 346-350. [CrossRef] [PubMed]
44. Thieringer, H.A, Jones, P.G, Inouye, M. Cold shock and adaptation. BioEssays 1998, 20, 49-57. [CrossRef]
45. De Angelis, M, di Cagno, R, Huet, C, Crecchio, C, Fox, P.F, Gobbetti, M. Heat shock response in Lactobacillus plantarum. Appl. Environ. Microbiol. 2004, 70, 1336-1346. [CrossRef] [PubMed]
46. Song, S, Bae, D.-W, Lim, K, Griffiths, M.W, Oh, S. Cold stress improves the ability of Lactobacillus plantarum L67 to survive freezing. Int. J. Food Microbiol. 2014, 191, 135-143. [CrossRef] [PubMed]
47. Fang, S.H, Lai, Y.J, Chou, C.C. The susceptibility of Streptococcus thermophilus 14085 to organic acid, simulated gastric juice, bile salt and disinfectant as influenced by cold shock treatment. Food Microbiol. 2013, 33, 55-60. [CrossRef] [PubMed]
48. Lourens-Hattingh, A, Viljoen, B.C. Yogurt as probiotic carrier food. Int. Dairy J. 2001, 11, 1-17. [CrossRef]
49. Desmond, C, Fitzgerald, G.F, Stanton, C, Ross, R.P. Improved stress tolerance of groesl-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl. Environ. Microbiol. 2004, 70, 5929-5936. [CrossRef] [PubMed]
50. Russo, P, Iturria, I, Mohedano, M.L, Caggianiello, G, Rainieri, S, Fiocco, D, Angel Pardo, M, Lopez, P, Spano, G. Zebrafish gut colonization by mcherry-labelled lactic acid bacteria. Appl. Microbiol. Biotechnol. 2015, 99, 3479-3490. [CrossRef] [PubMed]
51. Hidalgo-Cantabrana, C, Sanchez, B, Milani, C, Ventura, M, Margolles, A, Ruas-Madiedo, P. Genomic overview and biological functions of exopolysaccharide biosynthesis in bifidobacterium spp. Appl. Environ. Microbiol. 2014, 80, 9-18. [CrossRef] [PubMed]
52. Desmond, C, Ross, R.P, O’Callaghan, E, Fitzgerald, G, Stanton, C. Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia. J. Appl. Microbiol. 2002, 93, 1003-1011. [CrossRef] [PubMed]
53. Gouesbet, G, Jan, G, Boyaval, P. Lactobacillus delbrueckii ssp. Bulgaricus thermotolerance. Lait 2001, 81, 301-309. [CrossRef]
54. Phadtare, S, Alsina, J, Inouye, M. Cold-shock response and cold-shock proteins. Curr. Opin. Microbiol. 1999, 2, 175-180. [CrossRef]
55. Šeme, H, Gjuračić, K, Kos, B, Fujs, Š, Štempelj, M, Petković, H, Šušković, J, Bogovič Matijašić, B, Kosec, G. Acid resistance and response to pH-induced stress in two Lactobacillus plantarum strains with probiotic potential. Benef. Microb. 2014, 6, 369-379. [CrossRef] [PubMed]
56. Sánchez, B, Champomier-Vergès, M.-C, Collado, M.D.C, Anglade, P, Baraige, F, Sanz, Y, delos Reyes-Gavilán, C.G, Margolles, A, Zagorec, M. Low-pH adaptation and the acid tolerance response of bifidobacterium longum biotype longum. Appl. Environ. Microbiol. 2007, 73, 6450-6459. [CrossRef] [PubMed]
57. Collado, M.C, Sanz, Y. Induction of acid resistance in bifidobacterium: A mechanism for improving desirable traits of potentially probiotic strains. J. Appl. Microbiol. 2007, 103, 1147-1157. [CrossRef] [PubMed]
58. He, T, Priebe, M.G, Zhong, Y, Huang, C, Harmsen, H.J.M, Raangs, G.C, Antoine, J.M, Welling, G.W, Vonk, R.J. Effects of yogurt and bifidobacteria supplementation on the colonic microbiota in lactose-intolerant subjects. J. Appl. Microbiol. 2008, 104, 595-604. [CrossRef] [PubMed]
59. Jin, J, Zhang, B, Guo, H, Cui, J, Jiang, L, Song, S, Sun, M, Ren, F. Mechanism analysis of acid tolerance response of Bifidobacterium longum subsp. Longum BBMN 68 by gene expression profile using RNA-sequencing. PLoS ONE 2012, 7, e50777.
60. Palmfeldt, J, Hahn-Hägerdal, B. Influence of culture ph on survival of Lactobacillus reuteri subjected to freeze-drying. Int. J. Food Microbiol. 2000, 55, 235-238. [CrossRef]
61. Mathipa, M, Thantsha, M. Cocktails of probiotics pre-adapted to multiple stress factors are more robust under simulated gastrointestinal conditions than their parental counterparts and exhibit enhanced antagonistic capabilities against Escherichia coli and Staphylococcus aureus. Gut Pathog. 2015, 7, 5. [CrossRef] [PubMed]
62. Lourens-Hattingh, A, Viljoen, B.C. Growth and survival of a probiotic yeast in dairy products. Food Res. Int. 2001, 34, 791-796. [CrossRef]
63. Gaudreau, H, Champagne, C.P, Remondetto, G.E, Alvarez, P.A, Gomaa, A, Subirade, M. Tea extract render probiotic Lactobacillus helveticus more resistant to oxygen exposure through lipid modification mechanism. Food Res. Int. 2016, 81, 141-148. [CrossRef]
64. Gaudreau, H, Champagne, C.P, Remondetto, G.E, Bazinet, L, Subirade, M. Effect of catechins on the growth of oxygen-sensitive probiotic bacteria. Food Res. Int. 2013, 53, 751-757. [CrossRef]
65. Kailasapathy, K. Microencapsulation of probiotic bacteria technology and potential applications. Curr. Issues Intest. Microbiol. 2002, 3, 39-48. [PubMed]
66. Rallu, F, Gruss, A, Ehrlich, S.D, Maguin, E. Acid-and multistress-resistant mutants of Lactococcus lactis: Identification of intracellular stress signals. Mol. Microbiol. 2000, 35, 517-528. [CrossRef] [PubMed]
67. Bergmaier, D, Champagne, C.P, Lacroix, C. Growth and exopolysaccharide production during free and immobilized cell chemostat culture of Lactobacillus rhamnosus rw-9595m. J. Appl. Microbiol. 2005, 98, 272-284. [CrossRef] [PubMed]
68. Ninomiya, K, Matsuda, K, Kawahata, T, Kanaya, T, Kohno, M, Katakura, Y, Asada, M, Shioya, S. Effect of CO2 concentration on the growth and exopolysaccharide production of Bifidobacterium longum cultivated under anaerobic conditions. J. Biosci. Bioeng. 2009, 107, 535-537. [CrossRef] [PubMed]
69. Ebel, B, Martin, F, Le, L.D, Gervais, P, Cachon, R. Use of gases to improve survival of Bifidobacterium bifidum by modifying redox potential in fermented milk. J. Dairy Sci. 2011, 94, 2185-2191. [CrossRef] [PubMed]
70. Bolduc, M.-P, Raymond, Y, Fustier, P, Champagne, C.P, Vuillemard, J.-C. Sensitivity of bifidobacteria to oxygen and redox potential in non-fermented pasteurized milk. Int. Dairy J. 2006, 16, 1038-1048. [CrossRef]
71. Kawasaki, S, Nagasaku, M, Mimura, T, Katashima, H, Ijyuin, S, Satoh, T, Niimura, Y. Effect of CO2 on colony development by bifidobacterium species. Appl. Environ. Microbiol. 2007, 73, 7796-7798. [CrossRef] [PubMed]
72. Arioli, S, Roncada, P, Salzano, A.M, Deriu, F, Corona, S, Guglielmetti, S, Bonizzi, L, Scaloni, A, Mora, D. The relevance of carbon dioxide metabolism in Streptococcus thermophilus. Microbiology 2009, 155, 1953-1965. [CrossRef] [PubMed]
73. Arioli, S, Monnet, C, Guglielmetti, S, Parini, C, De Noni, I, Hogenboom, J, Halami, P.M, Mora, D. Aspartate biosynthesis is essential for the growth of Streptococcus thermophilus in milk, and aspartate availability modulates the level of urease activity. Appl. Environ. Microbiol. 2007, 73, 5789-5796. [CrossRef] [PubMed]
74. Nicoloff, H, Elagoz, A, Arsene-Ploetze, F, Kammerer, B, Martinussen, J, Bringel, F. Repression of the pyr operon in Lactobacillus plantarum prevents its ability to grow at low carbon dioxide levels. J. Bacteriol. 2005, 187, 2093-2104. [CrossRef] [PubMed]
75. Nicoloff, H, Hubert, J.C, Bringel, F. In Lactobacillus plantarum, carbamoyl phosphate is synthesized by two carbamoyl-phosphate synthetases (CPS): Carbon dioxide differentiates the Arginine-repressed from the pyrimidine-regulated cps. J. Bacteriol. 2000, 182, 3416-3422. [CrossRef] [PubMed]
76. Nicoloff, H, Hubert, J.-C, Bringel, F. Carbamoyl-phosphate synthetases (CPS) in lactic acid bacteria and other Gram-positive bacteria. Lait 2001, 81, 151-159. [CrossRef]
77. Bolotin, A, Quinquis, B, Renault, P, Sorokin, A, Ehrlich, S.D, Kulakauskas, S, Lapidus, A, Goltsman, E, Mazur, M, Pusch, G.D, et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 2004, 22, 1554-1558. [CrossRef] [PubMed]
78. Shobharani, P, Prakash, M, Halami, P.M. Probiotic bacillus spp. In soy-curd: Nutritional, rheological, sensory, and antioxidant properties. J. Food Sci. 2015, 80, M2247-M2256. [CrossRef] [PubMed]
79. Ma, C, Ma, A, Gong, G, Liu, Z.; Wu, Z, Guo, B, Chen, Z. Cracking Streptococcus thermophilus to stimulate the growth of the probiotic Lactobacillus casei in co-culture. Int. J. Food Microbiol. 2015, 210, 42-46. [CrossRef] [PubMed]
80. Xie, N, Zhou, T, Li, B. Kefir yeasts enhance probiotic potentials of Lactobacillus paracasei h9: The positive effects of coaggregation between the two strains. Food Res. Int. 2012, 45, 394-401. [CrossRef]
81. Altieri, C, Bevilacqua, A, D’Amato, D, Nobile, M.A, Sinigaglia, M. Modelling the survival of starter lactic acid bacteria and Bifidobacterium bifidum in single and simultaneous cultures. Food Microbiol. 2008, 25, 729-734. [CrossRef] [PubMed]
82. Meng, X.C, Stanton, C, Fitzgerald, G.F, Daly, C, Ross, R.P. Anhydrobiotics: The challenges of drying probiotic cultures. Food Chem. 2008, 106, 1406-1416. [CrossRef]
83. 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. [PubMed]
84. Derzelle, S, Hallet, B, Ferain, T, Delcour, J, Hols, P. Improved adaptation to cold-shock, stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Appl. Environ. Microbiol. 2003, 69, 4285-4290. [CrossRef] [PubMed]
85. Ventura, M, Reniero, R, Zink, R. Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach. Appl. Environ. Microbiol. 2001, 67, 2760-2765. [CrossRef] [PubMed]
86. Talwalkar, A, Kailasapathy, K. Metabolic and biochemical responses of probiotic bacteria to oxygen. J. Dairy Sci. 2003, 86, 2537-2546. [CrossRef]
87. Cronin, M, Ventura, M, Fitzgerald, G.F, van Sinderen, D. Progress in genomics, metabolism and biotechnology of bifidobacteria. Int. J. Food Microbiol. 2011, 149, 4-18. [CrossRef] [PubMed]
88. Long, G, Zhu, P, Shen, Y, Tong, M. Influence of extracellular polymeric substances (EPS) on deposition kinetics of bacteria. Environ. Sci. Technol. 2009, 43, 2308-2314. [CrossRef] [PubMed]
89. Fu, N, Chen, X.D. Towards a maximal cell survival in convective thermal drying processes. Food Res. Int. 2011, 44, 1127-1149. [CrossRef]
90. Santivarangkna, C, Higl, B, Foerst, P. Protection mechanisms of sugars during different stages of preparation process of dried lactic acid starter cultures. Food Microbiol. 2008, 25, 429-441. [CrossRef] [PubMed]
91. Looijesteijn, P.J, Trapet, L, de Vries, E, Abee, T, Hugenholtz, J. Physiological function of exopolysaccharides produced by Lactococcus lactis. Int. J. Food Microbiol. 2001, 64, 71-80. [CrossRef]
92. De Vuyst, L, Degeest, B. Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol. Rev. 1999, 23, 153-177. [CrossRef] [PubMed]
93. Degeest, B, Janssens, B, de Vuyst, L. Exopolysaccharide (EPS) biosynthesis by Lactobacillus sakei 0-1: Production kinetics, enzyme activities and EPS yields. J. Appl. Microbiol. 2001, 91, 470-477. [CrossRef] [PubMed]
94. Leroy, F, de Vuyst, L. Advances in production and simplified methods for recovery and quantification of exopolysaccharides for applications in food and health. J. Dairy Sci. 2016, 99, 1-10. [CrossRef] [PubMed]
95. De Vuyst, L, de Vin, F, Vaningelgem, F, Degeest, B. Recent developments in the biosynthesis and applications of heteropolysaccharides from lactic acid bacteria. Int. Dairy J. 2001, 11, 687-707. [CrossRef]
96. Welman, A.D, Maddox, I.S, Archer, R.H. Screening and selection of exopolysaccharide-producing strains of Lactobacillus delbrueckii subsp. Bulgaricus. J. Appl. Microbiol. 2003, 95, 1200-1206. [CrossRef] [PubMed]
97. Dal Bello, F, Walter, J, Hertel, C, Hammes, W.P. In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst. Appl. Microbiol. 2001, 24, 232-237. [CrossRef] [PubMed]
98. Jolly, L, Vincent, S.F, Duboc, P, Neeser, J.-R. Exploiting exopolysaccharides from lactic acid bacteria. Anton. Leeuwenhoek 2002, 82, 367-374. [CrossRef]
99. Harutoshi, T. Exopolysaccharides of Lactic Acid Bacteria for Food and Colon Health Applications; INTECH Open Access Publisher: Rijeka, Croatia, 2013.
100. Péant, B, LaPointe, G, Gilbert, C, Atlan, D.; Ward, P, Roy, D. Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology 2005, 151, 1839-1851. [CrossRef] [PubMed]
101. Guillaume, E, Berger, B, Affolter, M, Kussmann, M. Label-free quantitative proteomics of two bifidobacterium longum strains. J. Proteom. 2009, 72, 771-784. [CrossRef] [PubMed]
102. Leiversa, S.H.-C.C, Robinsona, G, Margollesb, A, Ruas-Madiedob, P, Lawsa, A.P. Structure of the high molecular weight exopolysaccharide produced by Bifidobacterium animalissubsp. Lactis IPLA-R1 and sequence analysis of its putative epscluster. Carbohydr. Res. 2011, 346, 2710-2717. [CrossRef] [PubMed]
103. Fanning, S, Hall, L.J, Cronin, M, Zomer, A, MacSharry, J, Goulding, D, O’Connell Motherway, M, Shanahan, F, Nally, K, Dougan, G, et al. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc. Natl. Acad. Sci. USA 2012, 109, 2108-2113. [CrossRef] [PubMed]
104. Hidalgo-Cantabrana, C, Sanchez, B, Milani, C, Ventura, M, Margolles, A, Ruas-Madiedo, P. Exopolysaccharide biosynthesis in bifidobacterium spp.: Biological functions and a genomic overview. Appl. Environ. Microbiol. 2013. [CrossRef] [PubMed]
105. Sutherland, I. Biofilm exopolysaccharides: A strong and sticky framework. Microbiology 2001, 147, 3-9. [CrossRef] [PubMed]
106. Patel, S, Majumder, A, Goyal, A. Potentials of exopolysaccharides from lactic acid bacteria. Indian J. Microbiol. 2012, 52, 3-12. [CrossRef] [PubMed]
107. Ruas-Madiedo, P, Tuinier, R, Kanning, M, Zoon, P. Role of exopolysaccharides produced by Lactococcus lactis subsp. Cremoris on the viscosity of fermented milks. Int. Dairy J. 2002, 12, 689-695. [CrossRef]
108. Carvalho, A.S, Silva, J, Ho, P, Teixeira, P, Malcata, F.X, Gibbs, P. Protective effect of sorbitol and monosodium glutamate during storage of freeze-dried lactic acid bacteria. Le Lait 2003, 83, 203-210. [CrossRef]
109. Flemming, H.C, Neu, T.R, Wozniak, D.J. The EPS matrix: The “house of biofilm cells”. J. Bacteriol. 2007, 189, 7945-7947. [CrossRef] [PubMed]
110. Marx, J.G, Carpenter, S.D, Deming, J.W. Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34 h under extreme conditions. Can. J. Microbiol. 2009, 55, 63-72. [CrossRef] [PubMed]
111. Mozzi, F, Savoy de Giori, G, Font de Valdez, G. Udp-galactose 4-epimerase: A key enzyme in exopolysaccharide formation by Lactobacillus casei CRL 87 in controlled pH batch cultures. J. Appl. Microbiol. 2003, 94, 175-183. [CrossRef] [PubMed]
112. Öner, E.T. Microbial production of extracellular polysaccharides from biomass. In Pretreatment Techniques for Biofuels and Biorefineries; Fang, Z., Ed, Springer Berlin Heidelberg: Berlin, Germany, 2013; pp. 35-56.
113. Osman, A, Tzortzis, G, Rastall, R.A, Charalampopoulos, D. Bbgiv is an important bifidobacterium β-galactosidase for the synthesis of prebiotic galactooligosaccharides at high temperatures. J. Agric. Food Chem. 2011, 60, 740-748. [CrossRef] [PubMed]
114. Tymczyszyn, E.E, Sosa, N, Gerbino, E, Hugo, A, Gómez-Zavaglia, A, Schebor, C. Effect of physical properties on the stability of lactobacillus bulgaricus in a freeze-dried galacto-oligosaccharides matrix. Int. J. Food Microbiol. 2012, 155, 217-221. [CrossRef] [PubMed]
115. Santos, E.G, Costa, F.G.P, Silva, J.H.V, Martins, T.D.D, Figueiredo-Lima, D.F, Macari, M, Oliveira, C.J.B, Givisiez, P.E.N. Protective effect of mannan oligosaccharides against early colonization by salmonella enteritidis in chicks is improved by higher dietary threonine levels. J. Appl. Microbiol. 2013, 114, 1158-1165. [CrossRef] [PubMed]
116. Nandal, K, Sehrawat, A.R, Yadav, A.S, Vashishat, R.K, Boora, K.S. High temperature-induced changes in exopolysaccharides, lipopolysaccharides and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol. Res. 2005, 160, 367-373. [CrossRef] [PubMed]
117. Hongpattarakere, T, Cherntong, N, Wichienchot, S, Kolida, S, Rastall, R.A. In vitro prebiotic evaluation of exopolysaccharides produced by marine isolated lactic acid bacteria. Carbohydr. Polym. 2012, 87, 846-852. [CrossRef]
118. Ruijssenaars, H.J, Stingele, F, Hartmans, S. Biodegradability of food-associated extracellular polysaccharides. Curr. Microbiol. 2000, 40, 194-199. [CrossRef] [PubMed]
119. Mårtensson, O, Biörklund, M, Lambo, A.M, Dueñas-Chasco, M, Irastorza, A, Holst, O, Norin, E, Welling, G, Öste, R, Önning, G. Fermented, ropy, OAT-based products reduce cholesterol levels and stimulate the bifidobacteria flora in humans. Nutr. Res. 2005, 25, 429-442. [CrossRef]
120. Leroy, F, de Vuyst, L. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 2004, 15, 67-78. [CrossRef]
121. Guergoletto, K.B, Magnani, M, Martin, J.S, Andrade, C.G.T.J, Garcia, S. Survival of Lactobacillus casei (LC-1) adhered to prebiotic vegetal fibers. Innov. Food Sci. Emerg. Technol. 2010, 11, 415-421. [CrossRef]
122. Santivarangkna, C, Kulozik, U, Foerst, P. Inactivation mechanisms of lactic acid starter cultures preserved by drying processes. J. Appl. Microbiol. 2008, 105, 1-13. [CrossRef] [PubMed]
123. Gourbeyre, P, Denery, S, Bodinier, M. Probiotics, prebiotics, and synbiotics: Impact on the gut immune system and allergic reactions. J. Leukoc. Biol. 2011, 89, 685-695. [CrossRef] [PubMed]
124. Schrezenmeir, J, de Vrese, M. Probiotics, prebiotics, and synbiotics—Approaching a definition. Am. J. Clin. Nutr. 2001, 73, 361s-364s. [PubMed]
125. Wollowski, I, Rechkemmer, G, Pool-Zobel, B.L. Protective role of probiotics and prebiotics in colon cancer. Am. J. Clin. Nutr. 2001, 73, 451s-455s. [PubMed]
126. Gomi, A, Harima-Mizusawa, N, Shibahara-Sone, H, Kano, M, Miyazaki, K, Ishikawa, F. Effect of Bifidobacterium bifidum BF-1 on gastric protection and mucin production in an acute gastric injury rat model. J. Dairy Sci. 2012, 96, 832-837. [CrossRef] [PubMed]
127. Fanning, S, Hall, L.J, van Sinderen, D. Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection. Gut Microb. 2012, 3, 420-425. [CrossRef] [PubMed]
128. Conover, M.S, Sloan, G.P, Love, C.F, Sukumar, N, Deora, R. The bps polysaccharide of bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin. Mol. Microbiol. 2010, 77, 1439-1455. [CrossRef] [PubMed]