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Research article

Synthesis of β-Galactooligosaccharide Using Bifidobacterial β-Galactosidase Purified from Recombinant Escherichia coli

So Young Oh 1, So Youn Youn , Myung Soo Park , Hyoung-Geun Kim , Nam-In Baek , Zhipeng Li and Geun Eog Ji *

Department of Food and Nutrition, Research Institute of Human Ecology, Seoul National University, Republic of Korea, 1Research Center, BIFIDO Co. Ltd., Republic of Korea, 2Department of Hotel Culinary Art, Yeonsung University, Republic of Korea, 3Graduate School of Biotechnology and Oriental Medicine Biotechnology, Kyung Hee University, Republic of Korea

Received: February 23, 2017; Accepted: April 28, 2018

J. Microbiol. Biotechnol. 2017; 27(8): 1392-1400

Published August 28, 2017 https://doi.org/10.4014/jmb.1702.02058

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Galactooligosaccharides (GOSs) are known to be selectively utilized by Bifidobacterium, which can bring about healthy changes of the composition of intestinal microflora. In this study, β-GOS were synthesized using bifidobacterial β-galactosidase (G1) purified from recombinant E. coli with a high GOS yield and with high productivity and enhanced bifidogenic activity. The purified recombinant G1 showed maximum production of β-GOSs at pH 8.5 and 45oC. A matrix-assisted laser desorption ionization time-of-flight mass spectrometry analysis of the major peaks of the produced β-GOSs showed MW of 527 and 689, indicating the synthesis of β-GOSs at degrees of polymerization (DP) of 3 and DP4, respectively. The trisaccharides were identified as β-D-galactopyranosyl-(1→4)-O-β-D-galactopyranosyl-(1→4)-O-β-D-glucopyranose, and the tetrasaccharides were identified as β-D-galactopyranosyl-(1→4)-O-β-D-galactopyranosyl- (1→4)-O-β-D-galactopyranosyl-(1→4)-O-β-D-glucopyranose. The maximal production yield of GOSs was as high as 25.3% (w/v) using purified recombinant β-galactosidase and 36% (w/v) of lactose as a substrate at pH 8.5 and 45oC. After 140 min of the reaction under this condition, 268.3 g/l of GOSs was obtained. With regard to the prebiotic effect, all of the tested Bifidobacterium except for B. breve grew well in BHI medium containing β-GOS as a sole carbon source, whereas lactobacilli and Streptococcus thermophilus scarcely grew in the same medium. Only Bacteroides fragilis, Clostridium ramosum, and Enterobacter cloacae among the 17 pathogens tested grew in BHI medium containing β-GOS as a sole carbon source; the remaining pathogens did not grow in the same medium. Consequently, the β-GOS are expected to contribute to the beneficial change of intestinal microbial flora.

Keywords

β-Galactooligosaccharides, Bifidobacterium longum subsp. longum RD47, prebiotics, prebiotics, recombinant Escherichia coli

References

  1. Roberfroid M. 2007. Prebiotics: the concept revisited. J. Nutr. 137: 830S-837S.
    Pubmed CrossRef
  2. Osman A, Tzortzis G, Rastall RA, Charalampopoulos D. 2010. A comprehensive investigation of the synthesis of prebiotic galactooligosaccharides by whole cells of Bifidobacterium bifidum NCIMB 41171. J. Biotechnol. 150: 140-148.
    Pubmed CrossRef
  3. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB. 2004. Dietary modulation of the human colonic microbiota. Nutr. Res. Rev. 17: 259-275.
    Pubmed CrossRef
  4. Hsu C-A, Lee S-L, Chou C-C. 2007. Enzymatic production of galactooligosaccharides by β-galactosidase from Bifidobacterium longum BCRC 15708. J. Agric. Food Chem. 55: 2225-2230.
    Pubmed CrossRef
  5. Tzortzis G , Goulas A K, G ee JM, Gibson GR. 2 005. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J. Nutr. 135: 1726-1731.
    Pubmed CrossRef
  6. Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T, Rupnow J, et al. 2011. Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Curr. Microbiol. 62: 1448-1454.
    Pubmed CrossRef
  7. Sinclair HR, de Slegte J, Gibson GR, Rastall RA. 2009. Galactooligosaccharides (GOS) inhibit Vibrio cholerae toxin binding to its GM1 receptor. J. Agric. Food Chem. 57: 3113-3119.
    Pubmed CrossRef
  8. Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW. 2006. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect. Immun. 74: 6920-6928.
    Pubmed PMC CrossRef
  9. Searle LE, Cooley WA, Jones G, Nunez A, Crudgington B, Weyer U, et al. 2010. Purified galactooligosaccharide, derived from a mixture produced by the enzymic activity of Bifidobacterium bifidum, reduces Salmonella enterica serovar Typhimurium adhesion and invasion in vitro and in vivo. J. Med. Microbiol. 59: 1428-1439.
    Pubmed CrossRef
  10. Cardelle-Cobas A, Corzo N, Olano A, Peláez C, Requena T, Ávila M. 2011. Galactooligosaccharides derived from lactose and lactulose: influence of structure on Lactobacillus, Streptococcus and Bifidobacterium growth. Int. J. Food Microbiol. 149: 81-87.
    Pubmed CrossRef
  11. Vulevic J, Juric A, Tzortzis G, Gibson GR. 2013. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. J. Nutr. 143: 324-331.
    Pubmed CrossRef
  12. Vulevic J, Juric A, Walton GE, Claus SP, Tzortzis G, Toward RE, et al. 2015. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br. J. Nutr. 114: 586-595.
    Pubmed CrossRef
  13. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. 2008. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (BGOS) in healthy elderly volunteers. Am. J. Clin. Nutr. 88: 1438-1446.
  14. Silk D, Davis A, Vulevic J, Tzortzis G, Gibson G. 2009. Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment. Pharmacol. Ther. 29: 508-518.
    Pubmed CrossRef
  15. Li Z, Jin H, Oh SY, Ji GE. 2016. Anti-obese effects of two lactobacilli and two bifidobacteria on ICR mice fed on a high fat diet. Biochem. Biophys. Res. Commun. 480: 222-227.
    Pubmed CrossRef
  16. Iraporda C, Errea A, Romanin DE, Cayet D, Pereyra E, Pignataro O, et al. 2015. Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology 220: 1161-1169.
    Pubmed CrossRef
  17. Pan X-D, Chen F-Q, Wu T-X, Tang H-G, Zhao Z-Y. 2009. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J. Zhejiang Univ. Sci. B 10: 258-263.
    Pubmed PMC CrossRef
  18. Garrido D, Ruiz-Moyano S, Jimenez-Espinoza R, Eom H-J, Block DE, Mills DA. 2013. Utilization of galactooligosaccharides by Bifidobacterium longum subsp. infantis isolates. Food Microbiol. 33: 262-270.
    Pubmed PMC CrossRef
  19. Bakken AP, Hill CG, Amundson CH. 1989. Hydrolysis of lactose in skim milk by immobilized β-galactosidase in a spiral flow reactor. Biotechnol. Bioeng. 33: 1249-1257.
    Pubmed CrossRef
  20. Bakken AP, Hill CG, Amundson CH. 1992. Hydrolysis of lactose in skim milk by immobilized β-galactosidase (Bacillus circulans). Biotechnol. Bioeng. 39: 408-417.
    Pubmed CrossRef
  21. Chen W, Chen H, Xia Y, Zhao J, Tian F, Zhang H. 2008. Production, purification, and characterization of a potential thermostable galactosidase for milk lactose hydrolysis from Bacillus stearothermophilus. J. Dairy Sci. 91: 1751-1758.
    Pubmed CrossRef
  22. Gaur R, Pant H, Jain R, Khare S. 2006. Galacto-oligosaccharide synthesis by immobilized Aspergillus oryzae β-galactosidase. Food Chem. 97: 426-430.
    CrossRef
  23. Martínez-Villaluenga C, Cardelle-Cobas A, Corzo N, Olano A, Villamiel M. 2008. Optimization of conditions for galactooligosaccharide synthesis during lactose hydrolysis by β-galactosidase from Kluyveromyces lactis (Lactozym 3000 L HP G). Food Chem. 107: 258-264.
    CrossRef
  24. Urrutia P, Rodriguez-Colinas BR, Fernandez-Arrojo L, Ballesteros AO, Wilson L, Illanes AS, et al. 2013. Detailed analysis of galactooligosaccharides synthesis with βgalactosidase from Aspergillus oryzae. J. Agric. Food Chem. 61: 1081-1087.
    Pubmed CrossRef
  25. Oliveira C, Guimarães PM, Domingues L. 2011. Recombinant microbial systems for improved β-galactosidase production and biotechnological applications. Biotechnol. Adv. 29: 600-609.
    Pubmed CrossRef
  26. Tzortzis G, Goulas AK, Gibson GR. 2005. Synthesis of prebiotic galactooligosaccharides using whole cells of a novel strain, Bifidobacterium bifidum NCIMB 41171. Appl. Microbiol. Biotechnol. 68: 412-416.
    Pubmed CrossRef
  27. Rabiu BA, Jay AJ, Gibson GR, Rastall RA. 2001. Synthesis and fermentation properties of novel galacto-oligosaccharides by β-galactosidases from Bifidobacterium species. Appl. Environ. Microbiol. 67: 2526-2530.
    Pubmed PMC CrossRef
  28. Depeint F, Tzortzis G, Vulevic J, I'Anson K, Gibson GR. 2008. Prebiotic evaluation of a novel galactooligosaccharide mixture produced by the enzymatic activity of Bifidobacterium bifidum NCIMB 41171, in healthy humans: a randomized, double-blind, crossover, placebo-controlled intervention study. Am. J. Clin. Nutr. 87: 785-791.
    Pubmed CrossRef
  29. Osman A, Tzortzis G, Rastall RA, Charalampopoulos D. 2013. High yield production of a soluble bifidobacterial β-galactosidase (BbgIV) in E. coli DH5α with improved catalytic efficiency for the synthesis of prebiotic galactooligosaccharides. J. Agric. Food Chem. 61: 2213-2223.
    Pubmed CrossRef
  30. Han YR, Youn SY, Ji GE, Park MS. 2014. Production of α- and β-galactosidases from Bifidobacterium longum subsp. longum RD47. J. Microbiol. Biotechnol. 24: 675-682.
    Pubmed CrossRef
  31. Vigsnaes LK, Nakai H, Hemmingsen L, Andersen JM, Lahtinen SJ, Rasmussen LE, et al. 2013. In vitro growth of four individual human gut bacteria on oligosaccharides produced by chemoenzymatic synthesis. Food Funct. 4: 784-793.
    Pubmed CrossRef
  32. Fai AEC, da Silva JB, de Andrade CJ, Bution ML, Pastore GM. 2014. Production of prebiotic galactooligosaccharides from lactose by Pseudozyma tsukubaensis and Pichia kluyveri. Biocatal. Agric. Biotechnol. 3: 343-350.
    CrossRef
  33. Yu L, O’Sullivan D. 2014. Production of galactooligosaccharides using a hyperthermophilic β-galactosidase in permeabilized whole cells of Lactococcus lactis. J. Dairy Sci. 97: 694-703.
    Pubmed CrossRef
  34. Hinz SW, Van den Broek LA, Beldman G, Vincken J-P, Voragen A G. 2 004. β-Galactosidase from Bifidobacterium adolescentis DSM20083 prefers β(1,4)-galactosides over lactose. Appl. Microbiol. Biotechnol. 66: 276-284.
    Pubmed CrossRef
  35. Hung M-N, Lee B. 2002. Purification and characterization of a recombinant β-galactosidase with transgalactosylation activity from Bifidobacterium infantis HL96. Appl. Microbiol. Biotechnol. 58: 439-445.
    Pubmed CrossRef
  36. Dumortier V, Brassart C, Bouquelet S. 1994. Purification and properties of β-D-galactosidase from Bifidobacterium bifidum exhibiting a transgalactosylation reaction. Biotechnol. Appl. Biochem. 19: 341-354.
  37. Ji E-S, Park N-H, Oh D-K. 2005. Galacto-oligosaccharide production by a thermostable recombinant β-galactosidase from Thermotoga maritima. World J. Microbiol. Biotechnol. 21: 759-764.
    CrossRef
  38. Zheng P, Yu H, Sun Z, Ni Y, Zhang W, Fan Y, Xu Y. 2006. Production of galacto-oligosaccharides by immobilized recombinant β-galactosidase from Aspergillus candidus. Biotechnol. J. 1: 1464-1470.
    Pubmed CrossRef
  39. Sela DA. 2011. Bifidobacterial utilization of human milk oligosaccharides. Int. J. Food Microbiol. 149: 58-64.
    Pubmed CrossRef
  40. Zivkovic AM, German JB, Lebrilla CB, Mills DA. 2011. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. USA 108: 4653-4658.
    Pubmed PMC CrossRef
  41. Sela DA, Mills DA. 2010. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18: 298-307.
    Pubmed PMC CrossRef
  42. Courtin CM, Swennen K, Verjans P, Delcour JA. 2009. Heat and pH stability of prebiotic arabinoxylooligosaccharides, xylooligosaccharides and fructooligosaccharides. Food Chem. 112: 831-837.
    CrossRef
  43. Gourbeyre P, Desbuards N, Grémy G, Le Gall S, Champ M, Denery-Papini S, et al. 2012. Exposure to a galactooligosaccharides/inulin prebiotic mix at different developmental time points differentially modulates immune responses in mice. J. Agric. Food Chem. 60: 11942-11951.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(8): 1392-1400

Published online August 28, 2017 https://doi.org/10.4014/jmb.1702.02058

Copyright © The Korean Society for Microbiology and Biotechnology.

Synthesis of β-Galactooligosaccharide Using Bifidobacterial β-Galactosidase Purified from Recombinant Escherichia coli

So Young Oh 1, So Youn Youn , Myung Soo Park , Hyoung-Geun Kim , Nam-In Baek , Zhipeng Li and Geun Eog Ji *

Department of Food and Nutrition, Research Institute of Human Ecology, Seoul National University, Republic of Korea, 1Research Center, BIFIDO Co. Ltd., Republic of Korea, 2Department of Hotel Culinary Art, Yeonsung University, Republic of Korea, 3Graduate School of Biotechnology and Oriental Medicine Biotechnology, Kyung Hee University, Republic of Korea

Received: February 23, 2017; Accepted: April 28, 2018

Abstract

Galactooligosaccharides (GOSs) are known to be selectively utilized by Bifidobacterium, which
can bring about healthy changes of the composition of intestinal microflora. In this study,
β-GOS were synthesized using bifidobacterial β-galactosidase (G1) purified from recombinant
E. coli with a high GOS yield and with high productivity and enhanced bifidogenic activity.
The purified recombinant G1 showed maximum production of β-GOSs at pH 8.5 and 45oC. A
matrix-assisted laser desorption ionization time-of-flight mass spectrometry analysis of the
major peaks of the produced β-GOSs showed MW of 527 and 689, indicating the synthesis of
β-GOSs at degrees of polymerization (DP) of 3 and DP4, respectively. The trisaccharides were
identified as β-D-galactopyranosyl-(1→4)-O-β-D-galactopyranosyl-(1→4)-O-β-D-glucopyranose,
and the tetrasaccharides were identified as β-D-galactopyranosyl-(1→4)-O-β-D-galactopyranosyl-
(1→4)-O-β-D-galactopyranosyl-(1→4)-O-β-D-glucopyranose. The maximal production yield of
GOSs was as high as 25.3% (w/v) using purified recombinant β-galactosidase and 36% (w/v)
of lactose as a substrate at pH 8.5 and 45oC. After 140 min of the reaction under this condition,
268.3 g/l of GOSs was obtained. With regard to the prebiotic effect, all of the tested
Bifidobacterium except for B. breve grew well in BHI medium containing β-GOS as a sole carbon
source, whereas lactobacilli and Streptococcus thermophilus scarcely grew in the same medium.
Only Bacteroides fragilis, Clostridium ramosum, and Enterobacter cloacae among the 17 pathogens
tested grew in BHI medium containing β-GOS as a sole carbon source; the remaining
pathogens did not grow in the same medium. Consequently, the β-GOS are expected to
contribute to the beneficial change of intestinal microbial flora.

Keywords: β-Galactooligosaccharides, Bifidobacterium longum subsp. longum RD47, prebiotics, prebiotics, recombinant Escherichia coli

References

  1. Roberfroid M. 2007. Prebiotics: the concept revisited. J. Nutr. 137: 830S-837S.
    Pubmed CrossRef
  2. Osman A, Tzortzis G, Rastall RA, Charalampopoulos D. 2010. A comprehensive investigation of the synthesis of prebiotic galactooligosaccharides by whole cells of Bifidobacterium bifidum NCIMB 41171. J. Biotechnol. 150: 140-148.
    Pubmed CrossRef
  3. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB. 2004. Dietary modulation of the human colonic microbiota. Nutr. Res. Rev. 17: 259-275.
    Pubmed CrossRef
  4. Hsu C-A, Lee S-L, Chou C-C. 2007. Enzymatic production of galactooligosaccharides by β-galactosidase from Bifidobacterium longum BCRC 15708. J. Agric. Food Chem. 55: 2225-2230.
    Pubmed CrossRef
  5. Tzortzis G , Goulas A K, G ee JM, Gibson GR. 2 005. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J. Nutr. 135: 1726-1731.
    Pubmed CrossRef
  6. Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T, Rupnow J, et al. 2011. Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Curr. Microbiol. 62: 1448-1454.
    Pubmed CrossRef
  7. Sinclair HR, de Slegte J, Gibson GR, Rastall RA. 2009. Galactooligosaccharides (GOS) inhibit Vibrio cholerae toxin binding to its GM1 receptor. J. Agric. Food Chem. 57: 3113-3119.
    Pubmed CrossRef
  8. Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW. 2006. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect. Immun. 74: 6920-6928.
    Pubmed KoreaMed CrossRef
  9. Searle LE, Cooley WA, Jones G, Nunez A, Crudgington B, Weyer U, et al. 2010. Purified galactooligosaccharide, derived from a mixture produced by the enzymic activity of Bifidobacterium bifidum, reduces Salmonella enterica serovar Typhimurium adhesion and invasion in vitro and in vivo. J. Med. Microbiol. 59: 1428-1439.
    Pubmed CrossRef
  10. Cardelle-Cobas A, Corzo N, Olano A, Peláez C, Requena T, Ávila M. 2011. Galactooligosaccharides derived from lactose and lactulose: influence of structure on Lactobacillus, Streptococcus and Bifidobacterium growth. Int. J. Food Microbiol. 149: 81-87.
    Pubmed CrossRef
  11. Vulevic J, Juric A, Tzortzis G, Gibson GR. 2013. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. J. Nutr. 143: 324-331.
    Pubmed CrossRef
  12. Vulevic J, Juric A, Walton GE, Claus SP, Tzortzis G, Toward RE, et al. 2015. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br. J. Nutr. 114: 586-595.
    Pubmed CrossRef
  13. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. 2008. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (BGOS) in healthy elderly volunteers. Am. J. Clin. Nutr. 88: 1438-1446.
  14. Silk D, Davis A, Vulevic J, Tzortzis G, Gibson G. 2009. Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment. Pharmacol. Ther. 29: 508-518.
    Pubmed CrossRef
  15. Li Z, Jin H, Oh SY, Ji GE. 2016. Anti-obese effects of two lactobacilli and two bifidobacteria on ICR mice fed on a high fat diet. Biochem. Biophys. Res. Commun. 480: 222-227.
    Pubmed CrossRef
  16. Iraporda C, Errea A, Romanin DE, Cayet D, Pereyra E, Pignataro O, et al. 2015. Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology 220: 1161-1169.
    Pubmed CrossRef
  17. Pan X-D, Chen F-Q, Wu T-X, Tang H-G, Zhao Z-Y. 2009. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J. Zhejiang Univ. Sci. B 10: 258-263.
    Pubmed KoreaMed CrossRef
  18. Garrido D, Ruiz-Moyano S, Jimenez-Espinoza R, Eom H-J, Block DE, Mills DA. 2013. Utilization of galactooligosaccharides by Bifidobacterium longum subsp. infantis isolates. Food Microbiol. 33: 262-270.
    Pubmed KoreaMed CrossRef
  19. Bakken AP, Hill CG, Amundson CH. 1989. Hydrolysis of lactose in skim milk by immobilized β-galactosidase in a spiral flow reactor. Biotechnol. Bioeng. 33: 1249-1257.
    Pubmed CrossRef
  20. Bakken AP, Hill CG, Amundson CH. 1992. Hydrolysis of lactose in skim milk by immobilized β-galactosidase (Bacillus circulans). Biotechnol. Bioeng. 39: 408-417.
    Pubmed CrossRef
  21. Chen W, Chen H, Xia Y, Zhao J, Tian F, Zhang H. 2008. Production, purification, and characterization of a potential thermostable galactosidase for milk lactose hydrolysis from Bacillus stearothermophilus. J. Dairy Sci. 91: 1751-1758.
    Pubmed CrossRef
  22. Gaur R, Pant H, Jain R, Khare S. 2006. Galacto-oligosaccharide synthesis by immobilized Aspergillus oryzae β-galactosidase. Food Chem. 97: 426-430.
    CrossRef
  23. Martínez-Villaluenga C, Cardelle-Cobas A, Corzo N, Olano A, Villamiel M. 2008. Optimization of conditions for galactooligosaccharide synthesis during lactose hydrolysis by β-galactosidase from Kluyveromyces lactis (Lactozym 3000 L HP G). Food Chem. 107: 258-264.
    CrossRef
  24. Urrutia P, Rodriguez-Colinas BR, Fernandez-Arrojo L, Ballesteros AO, Wilson L, Illanes AS, et al. 2013. Detailed analysis of galactooligosaccharides synthesis with βgalactosidase from Aspergillus oryzae. J. Agric. Food Chem. 61: 1081-1087.
    Pubmed CrossRef
  25. Oliveira C, Guimarães PM, Domingues L. 2011. Recombinant microbial systems for improved β-galactosidase production and biotechnological applications. Biotechnol. Adv. 29: 600-609.
    Pubmed CrossRef
  26. Tzortzis G, Goulas AK, Gibson GR. 2005. Synthesis of prebiotic galactooligosaccharides using whole cells of a novel strain, Bifidobacterium bifidum NCIMB 41171. Appl. Microbiol. Biotechnol. 68: 412-416.
    Pubmed CrossRef
  27. Rabiu BA, Jay AJ, Gibson GR, Rastall RA. 2001. Synthesis and fermentation properties of novel galacto-oligosaccharides by β-galactosidases from Bifidobacterium species. Appl. Environ. Microbiol. 67: 2526-2530.
    Pubmed KoreaMed CrossRef
  28. Depeint F, Tzortzis G, Vulevic J, I'Anson K, Gibson GR. 2008. Prebiotic evaluation of a novel galactooligosaccharide mixture produced by the enzymatic activity of Bifidobacterium bifidum NCIMB 41171, in healthy humans: a randomized, double-blind, crossover, placebo-controlled intervention study. Am. J. Clin. Nutr. 87: 785-791.
    Pubmed CrossRef
  29. Osman A, Tzortzis G, Rastall RA, Charalampopoulos D. 2013. High yield production of a soluble bifidobacterial β-galactosidase (BbgIV) in E. coli DH5α with improved catalytic efficiency for the synthesis of prebiotic galactooligosaccharides. J. Agric. Food Chem. 61: 2213-2223.
    Pubmed CrossRef
  30. Han YR, Youn SY, Ji GE, Park MS. 2014. Production of α- and β-galactosidases from Bifidobacterium longum subsp. longum RD47. J. Microbiol. Biotechnol. 24: 675-682.
    Pubmed CrossRef
  31. Vigsnaes LK, Nakai H, Hemmingsen L, Andersen JM, Lahtinen SJ, Rasmussen LE, et al. 2013. In vitro growth of four individual human gut bacteria on oligosaccharides produced by chemoenzymatic synthesis. Food Funct. 4: 784-793.
    Pubmed CrossRef
  32. Fai AEC, da Silva JB, de Andrade CJ, Bution ML, Pastore GM. 2014. Production of prebiotic galactooligosaccharides from lactose by Pseudozyma tsukubaensis and Pichia kluyveri. Biocatal. Agric. Biotechnol. 3: 343-350.
    CrossRef
  33. Yu L, O’Sullivan D. 2014. Production of galactooligosaccharides using a hyperthermophilic β-galactosidase in permeabilized whole cells of Lactococcus lactis. J. Dairy Sci. 97: 694-703.
    Pubmed CrossRef
  34. Hinz SW, Van den Broek LA, Beldman G, Vincken J-P, Voragen A G. 2 004. β-Galactosidase from Bifidobacterium adolescentis DSM20083 prefers β(1,4)-galactosides over lactose. Appl. Microbiol. Biotechnol. 66: 276-284.
    Pubmed CrossRef
  35. Hung M-N, Lee B. 2002. Purification and characterization of a recombinant β-galactosidase with transgalactosylation activity from Bifidobacterium infantis HL96. Appl. Microbiol. Biotechnol. 58: 439-445.
    Pubmed CrossRef
  36. Dumortier V, Brassart C, Bouquelet S. 1994. Purification and properties of β-D-galactosidase from Bifidobacterium bifidum exhibiting a transgalactosylation reaction. Biotechnol. Appl. Biochem. 19: 341-354.
  37. Ji E-S, Park N-H, Oh D-K. 2005. Galacto-oligosaccharide production by a thermostable recombinant β-galactosidase from Thermotoga maritima. World J. Microbiol. Biotechnol. 21: 759-764.
    CrossRef
  38. Zheng P, Yu H, Sun Z, Ni Y, Zhang W, Fan Y, Xu Y. 2006. Production of galacto-oligosaccharides by immobilized recombinant β-galactosidase from Aspergillus candidus. Biotechnol. J. 1: 1464-1470.
    Pubmed CrossRef
  39. Sela DA. 2011. Bifidobacterial utilization of human milk oligosaccharides. Int. J. Food Microbiol. 149: 58-64.
    Pubmed CrossRef
  40. Zivkovic AM, German JB, Lebrilla CB, Mills DA. 2011. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. USA 108: 4653-4658.
    Pubmed KoreaMed CrossRef
  41. Sela DA, Mills DA. 2010. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18: 298-307.
    Pubmed KoreaMed CrossRef
  42. Courtin CM, Swennen K, Verjans P, Delcour JA. 2009. Heat and pH stability of prebiotic arabinoxylooligosaccharides, xylooligosaccharides and fructooligosaccharides. Food Chem. 112: 831-837.
    CrossRef
  43. Gourbeyre P, Desbuards N, Grémy G, Le Gall S, Champ M, Denery-Papini S, et al. 2012. Exposure to a galactooligosaccharides/inulin prebiotic mix at different developmental time points differentially modulates immune responses in mice. J. Agric. Food Chem. 60: 11942-11951.
    Pubmed CrossRef