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Evaluation of ginsenoside bioconversion of lactic acid bacteria isolated from kimchi

  • Park, Boyeon (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Hwang, Hyelyeon (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Lee, Jina (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Sohn, Sung-Oh (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Lee, Se Hee (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Jung, Min Young (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Lim, Hyeong In (Microbiology and Functionality Research Group, World Institute of Kimchi) ;
  • Park, Hae Woong (Advanced Process Technology and Fermentation Research Group, World Institute of Kimchi) ;
  • Lee, Jong-Hee (Microbiology and Functionality Research Group, World Institute of Kimchi)
  • Received : 2016.01.27
  • Accepted : 2016.10.05
  • Published : 2017.10.15

Abstract

Background: Panax ginseng is a physiologically active plant widely used in traditional medicine that is characterized by the presence of ginsenosides. Rb1, a major ginsenoside, is used as the starting material for producing ginsenoside derivatives with enhanced pharmaceutical potentials through chemical, enzymatic, or microbial transformation. Methods: To investigate the bioconversion of ginsenoside Rb1, we prepared kimchi originated bacterial strains Leuconostoc mensenteroides WiKim19, Pediococcus pentosaceus WiKim20, Lactobacillus brevis WiKim47, Leuconostoc lactis WiKim48, and Lactobacillus sakei WiKim49 and analyzed bioconversion products using LC-MS/MS mass spectrometer. Results: L. mesenteroides WiKim19 and Pediococcus pentosaceus WiKim20 converted ginsenoside Rb1 into the ginsenoside Rg3 approximately five times more than Lactobacillus brevis WiKim47, Leuconostoc lactis WiKim48, and Lactobacillus sakei WiKim49. L mesenteroides WIKim19 showed positive correlation with b-glucosidase activity and higher transformation ability of ginsenoside Rb1 into Rg3 than the other strains whereas, P. pentosaceus WiKim20 showed an elevated production of Rb3 even with lack of b-glucosidase activity but have the highest acidity among the five lactic acid bacteria (LAB). Conclusion: Ginsenoside Rg5 concentration of five LABs have ranged from ${\sim}2.6{\mu}g/mL$ to $6.5{\mu}g/mL$ and increased in accordance with the incubation periods. Our results indicate that the enzymatic activity along with acidic condition contribute to the production of minor ginsenoside from lactic acid bacteria.

Keywords

References

  1. Lin TY, Lin CW, Wang YJ. Linoleic acid isomerase activity in enzyme extracts from Lactobacillus acidophilus and Propionibacterium freudenreichii ssp. Shermanii. J Food Sci 2002;67:1502-5. https://doi.org/10.1111/j.1365-2621.2002.tb10312.x
  2. Setchell KD, Brown NM, Zimmer-Nechemias L, Brashear WT, Wolfe BE, Kirschner AS, Heubi JE. Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am J Clin Nutr 2002;76:447-53. https://doi.org/10.1093/ajcn/76.2.447
  3. Chun J, Kim GM, Lee KW, Choi ID, Kwon GH, Park JY, Jeong SJ, Kim JS, Kim JH. Conversion of isoflavone glucosides to aglycones in soymilk by fermentation with lactic acid bacteria. J Food Sci 2007a;72:M39-44. https://doi.org/10.1111/j.1750-3841.2007.00276.x
  4. Kim SH, Min JW, Quan LH, Lee S, Yang DU, Yang DC. Enzymatic transformation of ginsenoside Rb1 by Lactobacillus pentosus Strain 6105 from Kimchi. J Ginseng Res 2012;36:291-7. https://doi.org/10.5142/jgr.2012.36.3.291
  5. Quan LH, Piao JY, Min JW, Yang DU, Lee HN, Yang DC. Bioconversion of ginsenoside rb1 into compound k by Leuconostoc citreum LH1 isolated from kimchi. Braz J Microbiol 2011;42:1227-37. https://doi.org/10.1590/S1517-83822011000300049
  6. Kim DH. Chemical diversity of Panax ginseng, Panax quinquifolium, and Panax notoginseng. J Ginseng Res 2012;36:1-15. https://doi.org/10.5142/jgr.2012.36.1.1
  7. Yuan CS, Wang CZ, Wicks SM, Qi LW. Chemical and pharmacological studies of saponins with a focus on American ginseng. J Ginseng Res 2010;34:160-7. https://doi.org/10.5142/jgr.2010.34.3.160
  8. Cui CH, Kim JK, Kim SC, Im WT. Characterization of a ginsenosidetransforming beta-glucosidase from Paenibacillus mucilaginosus and its application for enhanced production of minor ginsenoside F(2). PLoS One 2014;9:e85727. https://doi.org/10.1371/journal.pone.0085727
  9. Choi S, Kim TW, Singh SV. Ginsenoside Rh2-mediated G1 phase cell cycle arrest in human breast cancer cells is caused by p15 Ink4B and p27 Kip1-dependent inhibition of cyclin-dependent kinases. Pharm Res 2009;26:2280-8. https://doi.org/10.1007/s11095-009-9944-9
  10. Choi JR, Hong SW, Kim Y, Jang SE, Kim NJ, Han MJ, Kim DH. Metabolic activities of ginseng and its constituents, ginsenoside rb1 and rg1, by human intestinal microflora. J Ginseng Res 2011;35:301-7. https://doi.org/10.5142/jgr.2011.35.3.301
  11. Kim M, Ahn BY, Lee JS, Chung SS, Lim S, Park SG, Jung HS, Lee HK, Park KS. The ginsenoside Rg3 has a stimulatory effect on insulin signaling in L6 myotubes. Biochem Biophys Res Commun 2009;389:70-3. https://doi.org/10.1016/j.bbrc.2009.08.088
  12. Leung KW, Wong AS. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5:20. https://doi.org/10.1186/1749-8546-5-20
  13. Park MW, Ha J, Chung SH. 20(S)-ginsenoside Rg3 enhances glucose-stimulated insulin secretion and activates AMPK. Biol Pharm Bull 2008;31:748-51. https://doi.org/10.1248/bpb.31.748
  14. Qi LW,Wang CZ, Yuan CS. Ginsenosides from American ginseng: chemical and pharmacological diversity. Phytochemistry 2011;72:689-99. https://doi.org/10.1016/j.phytochem.2011.02.012
  15. Shen H, Leung WI, Ruan JQ, Li SL, Lei JP, Wang YT, Yan R. Biotransformation of ginsenoside Rb1 via the gypenoside pathway by human gut bacteria. Chin Med 2013;8:22. https://doi.org/10.1186/1749-8546-8-22
  16. Bae EA, Choo MK, Park EK, Park SY, Shin HY, Kim DH. Metabolism of ginsenoside R(c) by human intestinal bacteria and its related antiallergic activity. Biol Pharm Bull 2002;25:743-7. https://doi.org/10.1248/bpb.25.743
  17. Kim KA, Jung IH, Park SH, Ahn YT, Huh CS, Kim DH. Comparative analysis of the gut microbiota in people with different levels of ginsenoside Rb1 degradation to compound K. PLoS One 2013;8:e62409. https://doi.org/10.1371/journal.pone.0062409
  18. Yang L, Deng Y, Xu S, Zeng X. In vivo pharmacokinetic and metabolism studies of ginsenoside Rd. J Chromatogr B Analyt Technol Biomed Life Sci 2007;854:77-84. https://doi.org/10.1016/j.jchromb.2007.04.014
  19. Hasegawa H, Sung J-H, Benno Y. Role of human intestinal Prevotella oris in hydrolyzing ginseng saponins. Planta Med 1997;63:436-40. https://doi.org/10.1055/s-2006-957729
  20. Kong H, Wang M, Venema K, Maathuis A, van der Heijden R, van der Greef J, Xu G, Hankemeier T. Bioconversion of red ginseng saponins in the gastro-intestinal tract in vitro model studied by high-performance liquid chromatography-high resolution Fourier transform ion cyclotron resonance mass spectrometry. J Chromatogr A 2009;1216:2195-203. https://doi.org/10.1016/j.chroma.2008.11.030
  21. Eom HJ, Seo DM, Han NS. Selection of psychrotrophic Leuconostoc spp. producing highly active dextransucrase from lactate fermented vegetables. Int J Food Microbiol 2007;117:61-7. https://doi.org/10.1016/j.ijfoodmicro.2007.02.027
  22. Islam MS, Choi H. Antidiabetic effect of Korean traditional Baechu (Chinese cabbage) kimchi in a type 2 diabetes model of rats. J Med Food 2009;12:292-7. https://doi.org/10.1089/jmf.2008.0181
  23. Yoo EJ, Lim HS, Park KO, Choi MR. Cytotoxic, antioxidative, and ACE inhibiting activities of Dolsan Leaf Mustard Juice (DLMJ) treated with lactic acid bacteria. Biotechno Bioprocess Eng 2005;10:60-6. https://doi.org/10.1007/BF02931184
  24. Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, Madsen EL, Jeon CO. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl Environ Microbiol 2011;77:2264-74. https://doi.org/10.1128/AEM.02157-10
  25. Cho YR, Chang JY, Chang HC. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol 2007;17:104-9.
  26. Kim JD. Antifungal activity of lactic acid bacteria isolated from Kimchi against Aspergillus fumigatus. Mycobiology 2005;33:210-4. https://doi.org/10.4489/MYCO.2005.33.4.210
  27. Jang SE, Han MJ, Kim SY, Kim DH. Lactobacillus plantarum CLP-0611 ameliorates colitis in mice by polarizing M1 to M2-like macrophages. Int Immunopharmacol 2014;21:186-92. https://doi.org/10.1016/j.intimp.2014.04.021
  28. Chang JY, Chang HC. Growth inhibition of foodborne pathogens by kimchi prepared with bacteriocin-producing starter culture. J Food Sci 2011;76:M72-8. https://doi.org/10.1111/j.1750-3841.2010.01965.x
  29. Seo BJ, Rather IA, Kumar VJ, Choi UH, Moon MR, Lim JH, Park YH. Evaluation of Leuconostoc mesenteroides YML003 as a probiotic against low-pathogenic avian influenza (H9N2) virus in chickens. J Appl Microbiol 2012;113:163-71. https://doi.org/10.1111/j.1365-2672.2012.05326.x
  30. Kim NH, Moon PD, Kim SJ, Choi IY, An HJ, Myung NY, Jeong HJ, Um JY, Hong SH, Kim HM. Lipid profile lowering effect of Soypro fermented with lactic acid bacteria isolated from Kimchi in high-fat diet-induced obese rats. Biofactors 2008;33:49-60. https://doi.org/10.1002/biof.5520330105
  31. Richard Y, Favier C, Oudar J. Differentiation of glucidolytic mycoplasmas isolated from goats by the API 50 CH system and electrophoresis. Ann Rech Vet. 1991;22:353-8.
  32. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW. EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 2007b;57:2259-61. https://doi.org/10.1099/ijs.0.64915-0
  33. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-80. https://doi.org/10.1093/nar/22.22.4673
  34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725-9. https://doi.org/10.1093/molbev/mst197
  35. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406-25.
  36. Kwon SW, Han SB, Park IH, Kim JM, Park MK, Park JH. Liquid chromatographic determination of less polar ginsenosides in processed ginseng. J Chromatogr A 2001;921:335-9. https://doi.org/10.1016/S0021-9673(01)00869-X
  37. Han BH, Park MH, Han YN, Woo LK, Sankawa U, Yahara S, Tanaka O. Degradation of ginseng saponins under mild acidic conditions. Planta Med 1982;44:146-9. https://doi.org/10.1055/s-2007-971425
  38. Ko SR, Choi KJ, Suzuki K, Suzuki Y. Enzymatic preparation of ginsenosides Rg2, Rh1, and F1. Chem Pharm Bull (Tokyo) 2003;51:404-8. https://doi.org/10.1248/cpb.51.404
  39. Chang KH, Jo MN, Kim KT, Paik HD. Evaluation of glucosidases of Aspergillus niger strain comparing with other glucosidases in transformation of ginsenoside Rb1 to ginsenosides Rg3. J Ginseng Res 2014;38:47-51. https://doi.org/10.1016/j.jgr.2013.11.008
  40. Huang D, Li Y, Zhang M, Ruan S, Zhang H, Wang Y, Hu P. Tartaric acid induced conversion of protopanaxadiol to ginsenosides Rg3 and Rg5 and their in situ recoveries by integrated expanded bed adsorption chromatography. J Sep Sci 2016;39:2995-3001. https://doi.org/10.1002/jssc.201600269

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