Whole-cell biocatalysis for producing ginsenoside rd from Rb1 using Lactobacillus rhamnosus GG

Journal of Microbiology and Biotechnology

Volumn 26, Issue 7, 2016, Pages 1206-1215

  Ku, Seockmo ^a,d   You, Hyun Ju ^a   Park, Myeong Soo ^b   Ji, Geun Eog ^a,b,c  

^a Seoul National University   (South Korea)

^b Yeonsung University   (South Korea)

^c Bifido Co   (South Korea)

^d PURDUE UNIVERSITY   (United States)

Author keywords

Biocatalysis; Ginsenoside; Lactobacillus rhamnosus; Whole cell bioconversion; glucosidase

Indexed keywords

BETA GLUCOSIDASE; CELLOBIOSE; GINSENOSIDE; GINSENOSIDE RB 1; GINSENOSIDE RD; PROBIOTIC AGENT; CULTURE MEDIUM;

ARTICLE; BACTERIAL STRAIN; BIOCATALYSIS; CELL DISRUPTION; CELL FREE SYSTEM; CELL SUSPENSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; FOOD INDUSTRY; GINSENG; LACTOBACILLUS RHAMNOSUS; NONHUMAN; PH MEASUREMENT; WHOLE CELL; BIOSYNTHESIS; CULTURE MEDIUM; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PANAX; PH;

BETA-GLUCOSIDASE; BIOCATALYSIS; CELLOBIOSE; CULTURE MEDIA; FERMENTATION; GINSENOSIDES; HYDROGEN-ION CONCENTRATION; LACTOBACILLUS RHAMNOSUS; PANAX;

EID: 84982275893     PISSN: 10177825     EISSN: 17388872     Source Type: Journal    
DOI: 10.4014/jmb.1601.01002     Document Type: Article

References (58)

1. Adachi N, Takahashi C, Ono-Murota N, Yamaguchi R, Tanaka T, Kondo A. 2013. Direct L-lysine production from cellobiose by Corynebacterium glutamicum displaying betaglucosidase on its cell surface. Appl. Microbiol. Biotechnol. 97: 7165-7172.
2. Adsul M, Khire J, Bastawde K, Gokhale D. 2007. Production of lactic acid from cellobiose and cellotriose by Lactobacillus delbrueckii mutant Uc-3. Appl. Environ. Microbiol. 73: 5055-5057.
3. nd Ed. Elsevier Inc., Burlington, MA.
4. Balejko E, Kucharska E, Balejko J. 2012. Influence of Lactobacillus rhamnosus gg methabolites on growth of periodontal diseases bacteria. Electron. J. Polish Agric. Univ. 15: 1-7.
5. rd Ed. Taylor & Francis CRC Press, Boca Raton, FL.
6. Chen Y, Nose M, Ogihara Y. 1987. Alkaline cleavage of ginsenoside. Chem. Pharm. Bull. (Tokyo) 35: 1653-1655.
7. Chi H, Ji GE. 2005. Transformation of ginsenosides Rb1 and Re from Panax ginseng by food microorganisms. Biotechnol. Lett. 27: 765-771.
8. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C. 2004. Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J. Appl. Microbiol. 96: 1024-1039.
9. Corcoran BM, Stanton C, Fitzgerald GF, Ross RP. 2005. Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl. Environ. Microbiol. 71: 3060-3067.
10. Difco. https://www.bd.com/europe/regulatory/Assets/IFU/Difco_BBL/288110.pdf. Accessed Dec. 20, 2015.
11. FDA. 2015. http://www.accessdata.fda.gov/scripts/fdcc/?set=GRASNotices&sort=Substance&order=ASC&search=. Accessed Dec. 20, 2015.
12. Food Safety and Sustainability Center. 2014. http://www.greenerchoices.org/pdf/cr_fsasc_gmo_final_report_10062014.pdf. Accessed Dec. 17, 2015.
13. Gao F, Zhang JM, Wang ZlG, Peng W, Hu HL, Fu CM. 2013. Biotransformation, a promising technology for anti-cancer drug development. Asian Pac. J. Cancer Prev. 14: 5599-5608.
14. Gielkens M, González-Candelas L, Sánchez-Torres P, van de Vondervoort P, de GraaV L, Visser J, Ramón D. 1999. The abfB gene encoding the major a-L-arabinofuranosidase of Aspergillus nidulans: nucleotide sequence, regulation and construction of a disrupted strain. Microbiology 145: 735-741.
15. Goldin BR, Gorbach SL, Saxelin M, Barakat S, Gualtieri L, Salminen S. 1992. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig. Dis. Sci 37: 121-128.
16. Gueimonde M, Noriega L, Margolles A, Reyes-Gavilán CG. 2007. Induction of a-L-arabinofuranosidase activity by monomeric carbohydrates in Bifidobacterium longum and ubiquity of encoding genes. Arch. Microbiol. 187: 145-153.
17. 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.
18. Hedberg M, Hasslöf P, Sjöström I, Twetman S, Stecksén-Blicks C. 2008. Sugar fermentation in probiotic bacteria – an in vitro study. Oral Microbiol. Immunol. 23: 482-485.
19. Hong H, Cui CH, Kim JK, Jin FX, Kim SC, Im WT. 2012. Enzymatic biotransformation of ginsenoside Rb1 and gypenoside XVII into ginsenosides Rd and F2 by recombinant β-glucosidase from Flavobacterium johnsoniae. J. Ginseng Res. 36: 418-424.
20. Hsueh HY, Yu B, Liu CT, Liu JR. 2014. Increase of the adhesion ability and display of a rumen fungal xylanase on the cell surface of Lactobacillus casei by using a listerial cellwall-anchoring protein. J. Sci. Food Agric. 94: 576-584.
21. Huang SJ, Chen MJ, Yueh PY, Yu B, Zhao X, Liu JR. 2011. Display of Fibrobacter succinogenes β-glucanase on the cell surface of Lactobacillus reuteri. J. Agric. Food Chem. 59: 1744-1751.
22. Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T. 1991. A human Lactobacillus strain (Lactobacillus casei sp. strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
23. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, et al. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. USA 40: 17193-171938.
24. Kim MS, Kwon B, Park MS, Ji GE. 2008. Isolation of ginsenoside Rh1 and compound K from fermented ginseng and efficacy assessment on systemic anaphylactic shock. Food Sci. Biotechnol. 17: 805-808.
25. Kim MS, Lee MS, Kim SH, Kim HJ, Sung MJ, Kim HY, et al. 2007. Anti-obesity effects of ginsenoside Rd via AMPK and PPAR gamma. Korean J. Biotechnol. Bioeng. 22: 341-344.
26. Kim RB. 2012. Consumer attitude of risk and benefits toward genetically modified (GM) foods in South Korea: implications for food policy. Eng. Econ. 23: 189-199.
27. Kim WK, Song SY, Oh WK, Kaewsuwan S, Tran TL, Kim WS, Sung JH. 2013. Wound-healing effect of ginsenoside Rd from leaves of Panax ginseng via cyclic AMP-dependent protein kinase pathway. Eur. J. Pharmacol. 702: 285-293.
28. Kok FS, Muhamad II, Lee CT, Razali F, Pa’e N, Shaharuddin S. 2012. Effects of pH and temperature on the growth and β-glucosidase activity of Lactobacillus rhamnosus NRRL 442 in anaerobic fermentation. Int. Rev. Biophys. Chem. (IREBIC) 3: 24-30.
29. Ku S, You HJ, Ji GE. 2009. Enhancement of anti-tumorigenic polysaccharide production, adhesion, and branch formation of Bifidobacterium bifidum BGN4 by phytic acid. Food Sci. Biotechnol.18: 749-754.
30. Ku S, You HJ, Park MS, Ji GE. 2015. Effects of ascorbic acid on α-L-arabinofuranosidase and α-L-arabinopyranosidase activities from Bifidobacterium longum RD47 and its application to whole cell bioconversion of ginsenoside. J. Korean Soc. Appl. Biol. Chem. 58: 857-865.
31. Ku S, Zheng H, Park MS, Ji GE. 2011. Optimization of β-glucuronidase activity from Lactobacillus delbrueckii Rh2 and its use for biotransformation of baicalin and wogonoside. J. Korean Soc. Appl. Biol. Chem. 54: 275-280.
32. Library of Congress. 2015. http://www.loc.gov/law/help/restrictions-on-gmos/eu.php#Opinion. Accessed Dec. 16, 2015.
33. Library of Congress. 2015. http://www.loc.gov/law/help/restrictions-on gmos/usa.php#Foodstuffs. Accessed Dec. 28, 2015.
34. Ma MF, Li SJ, Jin FX, Yu HS. 2012. Expression of ginsenoside glucosidase gene in E. coli and renaturation of inclusion body. J. Dalian Polytechnic Univ. 1: 004.
35. Matsuura M, Sasaki J, Murao S. 1995. Studies on β-glucosidases from soybeans that hydrolyze daidzin and genistin: isolation and characterization of an isozyme. Biosci. Biotechnol. Biochem. 59: 1623-1627.
36. Meurman JH, Antila H, Korhonen A, Salminen S. 1995. Effect of Lactobacillus rhamnosus strain GG (ATCC 53103) on the growth of Streptococcus sobrinus in vitro. Eur. J. Oral Sci. 103: 253-258.
37. Michlmayr H, Schümann C, Barreira Braz da Silva NM, Kulbe KD, Del Hierro AM. 2010. Isolation and basic characterization of a β-glucosidase from a strain of Lactobacillus brevis isolated from a malolactic starter culture. J. Appl. Microbiol. 108: 550-559.
38. Näse L, Hatakka K, Savilahti E, Saxelin M, Pönkä A, Poussa T, et al. 2001. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res. 35: 412-420.
39. Park CS, Yoo MH, Noh KH, Oh DK. 2012. Biotransformation of ginsenosides by hydrolyzing the sugar moieties of ginsenosides using microbial glycosidases. Appl. Environ. Microbiol. 87: 9-19.
40. Park SJ, Youn SY, Ji GE, Park MS. 2012. Whole cell biotransformation of major ginsenosides using leuconostocs and lactobacilli. Food Sci. Biotechnol. 21: 839-844.
41. Prather K. 2004. http://www.myoops.org/cocw/mit/NR/rdonlyres/Chemical-Engineering/10-492-2Fall-2004/684CA372-551B-4E59-88F1-4E338646E58A/0/lecture5.pdf. Accessed Dec. 17, 2015.
42. Quan K, Liu Q, Wan JY, Zhao YJ, Guo RZ, Alolga RN, et al. 2015. Rapid preparation of rare ginsenosides by acid transformation and their structure-activity relationships against cancer cells. Sci. Rep. 5: 8598.
43. Sanchez S, Demain, AL. 2008. Metabolic regulation and overproduction of primary metabolites. Microb. Biotechnol. 1: 283-319.
44. Saxelin M. 1997. Lactobacillus GG: a human probiotic strain with thorough clinical documentation. Food Rev. Int. 13: 293-313.
45. Schüürmann J, Quehl P, Festel G, Jose J. 2014. Bacterial whole-cell biocatalysts by surface display of enzymes: toward industrial application. Appl. Microbiol. Biotechnol. 98: 8031-8046.
46. Sestelo ABF, Poza M, Villa TG. 2004. β-Glucosidase activity in a Lactobacillus plantarum wine strain. World J. Microbiol. Biotechnol. 20: 633-637.
47. Singhvi M, Joshi D, Adsul M, Varma A, Gokhale D. 2010. D-(−)-Lactic acid production from cellobiose and cellulose by Lactobacillus lactis mutant RM2-24. Green Chem. 12: 1106-1109.
48. Smith MR, Khera E, Wen F. 2015. Engineering novel and improved biocatalysts by cell surface display. Ind. Eng. Chem. Res. 54: 4021-4032.
49. nd Edn. Elsevier Science Inc., Burlington, MA.
50. Tateno T, Fukuda H, Kondo A. 2007. Production of L-lysine from starch by Corynebacterium glutamicum displaying α-amylase on its cell surface. Appl. Microbiol. Biotechnol. 74: 1213-1220.
51. Tsuchiya A, Kobayashi G, Yamamoto H, Sekiguchi J. 1999. Production of a recombinant lipase artificially localized on the Bacillus subtilis cell surface. FEMS Microbiol. Lett. 176: 373-378.
52. van der Veen P, Arst HN Jr, Flipphi MJ, Visser J. 1994. Extracellular arabinases in Aspergillus nidulans: the effect of different cre mutations on enzyme levels. Arch. Microbiol. 162: 433-440.
53. Wakabayashi C, Hasegawa H, Murata J, Saiki I. 1997. In vivo antimetastatic action of ginseng protopanaxadiol saponins is based on their intestinal bacterial metabolites after oral administration. Oncol. Res. 9: 411-417.
54. Wang L, Zhang Y, Chen J, Li S, Wang Y, Hu, L, et al. 2012. Immunosuppressive effects of ginsenoside-Rd on skin allograft rejection in rats. J. Surg. Res. 176: 267-274.
55. Ximenes E, Kim Y, Mosier N, Dien B, Ladisch MR. 2011. Deactivation of cellulases by phenols. Enzyme Microb. Technol. 48: 54-60.
56. Xu C, Ji GE. 2013. Bioconversion of flavones during fermentation in milk containing Scutellaria baicalensis extract by Lactobacillus brevis. J. Microbiol. Biotechnol. 23: 1422-1427.
57. Yan Q, Zhou XW, Zhou W, Li XW, Feng MQ, Zhou P. 2008. Purification and properties of a novel beta-glucosidase, hydrolyzing ginsenoside Rb1 to CK, from Paecilomyces Bainier. J. Microbiol. Biotechnol. 18: 1081-1089.
58. Zhou JS, Wang JF, He BR, Cui YS, Fang XY, Ni JL, et al. 2014. Ginsenoside Rd attenuates mitochondrial permeability transition and cytochrome c release in isolated spinal cord mitochondria: involvement of kinase-mediated pathways. Int. J. Mol. Sci. 15: 9859-9877.