Biotransformation of major ginsenosides in ginsenosidemodel culture by lactic acid bacteria

Seong-Eun Park☆, Chang-Su Na☆, Seon-A Yoo, Seung-Ho Seo, Hong-Seok Son*

School of Oriental Medicine, Dongshin University, Naju, Jeonnam 520-714, Republic of Korea

☆These authors contributed equally to this work.

Supplemental Material

Table S1. (Supplemental Material)

The biotransformation pathways of PPD- and PPT-type ginsenosides.

Number1) / Microorganism / Pathway / Reference
1 / Aspergillusnigar / Rb1→Rd / Chang, Jo, Kim, & Paik (2014)
2 / Lactobacillus brevis / Rb1→Rd→F2→compound K / Yi, Lee, Yi, Cho, Park, & Kook (2012)
3 / Bifidobacterium sp. / Rb2,Rc→Rd→F2→compound K / Chi, Kim, & Ji (2005)
Lactobacillus delbruecii sp. / Rb2,Rc→Rd→F2→Rh2
Aspergillusnigar / Rb2→compoundO→compoundY→compound K
Rc→compoundMc→compound K
Aspergillususamii / Rb2→compound O→compoundY→compound K
4 / Bifidobacteriumlongum / Re→Rg2 / Choi et al. (2012)
5 / Bacillus sp. / Rc,Rb1,Rb2→Rd / Kim, Kim, & Cha (2007)
Lactococcuslactis
Lactobacillus sakei
Lactobacillus plantarum
Streptococcus pyogenes
Leuconostocgelidum
6 / Cellulosimicrobium sp. / Rb1→Rd→Rg3→Rh2→ppd / Na et al. (2009)
7 / Leuconostoccitreum / Rb1→Rd→F2→compound K / Quan, Piao, Min, Yang, Lee, & Yang (2011)
8 / Environmental DNA / Rb1→Rd / Kim et al. (2007)
9 / Sulfolobusacidocaldarius / Rb1→Rd
compound Y→compound K / Noh & Oh (2009)
10 / Culfolobussolfataricus / Rb1→Rd→F2→compound K
Rb2→Rd→F2→compound K
compound Mc→compound K / Noh, Son, Kim, & Oh (2009)
11 / Sphingomonas / Rb1→Gyp XVII
Rb2→compound O→F2
Rc→compoundMc1→F2
Rd→F2 / Wang et al. (2011)
12 / Bifidobacteriumlongum / Rb2→Rd
Rc→Rd / Lee, Hyun, & Kim (2011)
13 / Actinosynnemamirum / Rb1→Gyp XVII→Gyp LXXV
Rg3→Rh2→ppd
Rd→F2→Rh2→ppd
Rb2→compound O→compound Y
Rc→compound Mc1→compound Mc
Re→Rg2
Rg1→Rh1→ppt / Cui, Kim, & Im (2013)
14 / Lactobacillus brevis / Rd→F2→compound K / Quan et al. (2008)
15 / Thermuscaldophilus / Rb1,Rb2,Rc→Rd / Son, Kim, & Oh (2008)
16 / Microbacteriumesteraromaticum / Rb2→Rd→Rg3 / Quan, Wang, Jin, Wang, Kim, & Yang (2013)
17 / Paecilomycesbainier / Rb1→Rd / Ye et al. (2010)
18 / Paecilomycesbainier / Rb1→Rd→F2→compound K
Rb1→Gyp XVII
Rd→Rg3→Rh2 / Yan, Zhou, Shi, Zhou, Ju, & Feng (2010)
19 / Microbacterium sp. / Rb1→Rd→Rg3 / Cheng, Na, Bang, Kim, & Yang (2008)
20 / Bacteroides sp. / Re→Rg1→F1→ppt
Re→Rg2→Rh1→ppt
Rg1→Rh1 / Bae, Shin, & Kim (2005)
Bifidobacterium sp.
21 / Fusobacterium sp. / Rb1→Rd→F2→compound K
Rb1→Gyp XVII / Park, Bae, Sung, Lee, & Kim (2001)
22 / Aspergillusniger / Rf→Rh1 / Ruan et al. (2009)
23 / Leuconostocmesenteroides / Rb1→Gyp XVII
Rb1→Rd→F2→compound K / Quan et al. (2011)
24 / Flavobacterium johnsoniae / Rb1→Rd
Rb1→Gyp XVII / Hong, Cui, Kim, Jin, Kim, & Im (2012)
25 / Sanguibacterkeddieii / Rb1→GypXVII→GypLXXV→compound K
Rd→F2
Rg3→Rh2→PPD
Rb2→compound O→compound Y
Rc→compoundMc1→compound Mc
Re→Rg2
Rg1→F1 / Kim, Cui, Yoon, Kim, & Im (2012)
26 / Aspergillusniger / Rf→Rh1→ppt / Liu et al. (2010)
27 / Bifidobacterium sp. / Rb2,Rc→Rd→F2→compound K
Rb2,Rc→Rd→F2 / Chi, Lee, You, Park, & Ji (2006)
Lactobacillus delbrueckii / Rb2,Rc →Rd→F2→Rh2
Leuconostocparamesenteroides / Rb2,Rc→Rd→F2→Rh2
28 / Bacteroides sp. / Rc,Rb1,Rb2→Rg3→Rh2→ppd / Bae, Han, Choo, Park, & Kim (2002)
29 / Lactobacillus paralimentarius / Rb1→Gyp XVII→F2→compound K
Rb1→Rd →F2→compound K / Quan, Kim, Li, Choi, & Yang (2013)
30 / Microbacteriumesteraromaticum / Rg1→Rh1
Re→Rg2 / Quan, Min, Sathiyamoorthy, Yang, Kim, & Yang (2012)
31 / Fusariumsubglutinans / Rg1→F1 / Kim, Yoo, Lee, Choi, Kim, & Oh (2011)
32 / Leuconostoc sp. / F2→compound K / Park, Youn, Ji, & Park (2012)
Lactobacillus sp.

1)This is reference number of ginsenoside biotransformation pathways about Fig 1.

References

Bae, E. A., Han, M. J., Choo, M. K., Park, S. Y., & Kim, D. H. (2002).Metabolism of 20(S)-and 20(R)-ginsenoside Rg3 by human intestinal bacteria and its relation to in vitro biological activities.Biological andPharmaceutical Bulletin, 25, 58-63.

Bae, E. A., Shin, J. E., & Kim, D. H. (2005).Metabolism of ginsenoside Re by human intestinal microflora and its estrogenic effect.Biological and Pharmaceutical Bulletin, 28, 1903-1908.

Chang, K. H., Jo, M. N., Kim, K. T., & Paik, H. D. (2014). Evaluation of glucosidases of Aspergillusniger strain comparing with other glucosidases in transformation of ginsenoside Rb1 to ginsenosides Rg3. Journal of Ginseng Research, 38, 47-51.

Cheng, L. Q., Na, J. R., Bang, M. H., Kim, M. K., & Yang, D. C. (2008). Conversion of major ginsenoside Rb1 to 20(S)-ginsenoside Rg3 by Microbacterium sp. GS514.Phytochemistry, 69, 218-224.

Chi, H., Kim, D. H., & Ji, G. E. (2005). Transformation of ginsenosides Rb2 and Rc from Panax ginseng by food microorganisms. Biological and Pharmaceutical Bulletin, 28, 2102-2105.

Chi, H., Lee, B. H., You, H. J.,Park, M. S.,Ji, G. E. (2006). Differential transformation of ginsenosides from Panax ginseng by lactic acid bacteria.Journal of Microbiology and Biotechnology, 16, 1629-1633.

Choi, W. Y., Lee, C. G., Song, C. H., Seo, Y. C., Kim, J. S., Kim, B. H., et al. (2012). Enhancement of low molecular ginsenoside contents in low quality fresh ginseng by fermentation process. Korean Journal of Medicinal Crop Science, 20, 117-123.

Cui, C. H., Kim, S. C., & Im, W. T. (2013).Characterization of the ginsenoside-transforming recombinant β-glucosidase from Actinosynnemamirum and bioconversion of major ginsenosides into minor ginsenosides.Applied Microbiology and Biotechnology, 97, 649-659.

Hong, H., Cui, C. H., Kim, J. K., Jin, F. X., Kim, S. C., & Im, W. T. (2012). Enzymatic Biotransformation of Ginsenoside Rb1 and Gypenoside XVII into Ginsenosides Rd and F2 by Recombinant β-glucosidase from Flavobacteriumjohnsoniae.Journal of Ginseng Research, 36, 418-424.

Kim, H. G., Kim, K. Y., & Cha, C. J. (2007).Screening for ginseng-fermenting microorganisms capable of biotransformingginsenosides.The Korean Journal of Microbiology, 43, 142-146.

Kim, J. K., Cui, C. H., Yoon, M. H., Kim, S. C., & Im, W. T. (2012). Bioconversion of major ginsenosides Rg1 to minor ginsenoside F1 using novel recombinant ginsenoside hydrolyzing glycosidase cloned from Sanguibacterkeddieii and enzyme characterization. Journal of Biotechnology, 161, 294-301.

Kim, S. J., Lee, C. M., Kim, M. Y., Yeo, Y. S., Yoon, S. H., Kang, H. C., et al. (2007). Screening and characterization of an enzyme with beta-glucosidase activity from environmental DNA.Journal of Microbiology and Biotechnology, 17, 905-912.

Kim, Y. S., Yoo, M. H., Lee, G. W., Choi, J. G., Kim, K. R., & Oh, D. K. (2011). Ginsenoside F1 production from ginsenoside Rg1 by a purified β-glucosidase from Fusariummoniliforme var. subglutinans.Biotechnology letters, 33, 2457-2461.

Lee, J. H., Hyun, Y. J., & Kim, D. H. (2011).Cloning and characterization of α‐L‐arabinofuranosidase and bifunctional α‐L‐arabinopyranosidase/β‐D‐galactopyranosidase from Bifidobacteriumlongum H‐1.Journal of Applied Microbiology, 111, 1097-1107.

Liu, L., Gu, L. J., Zhang, D. L., Wang, Z., Wang, C. Y., Li, Z., et al. (2010). Microbial conversion of rare ginsenosideRf to 20(S)-protopanaxatriol by Aspergillusniger. Bioscience Biotechnology and Biochemistry, 74, 96-100.

Na, J. R., Kim, Y. J., Kim, S. H., Kim, H. B., Shim, J. S., Kim, S. Y., et al. (2009). Conversion of ginsenoside Rb1 by ginseng soil bacterium Cellulosimicrobiumsp. Gsoil 235 according to various culture broths.Korean Journal of Microbiology and Biotechnology, 37, 55-61.

Noh, K. H., & Oh, D. K. (2009). Production of the Rare Ginsenosides Compound K, Compound Y, and Compound Mc by a Thermostablebeta-Glycosidase from Sulfolobusacidocaldarius. Biological and Pharmaceutical Bulletin, 32, 1830-1835.

Noh, K. H., Son, J. W., Kim, H. J., & Oh, D. K. (2009).Ginsenoside compound K production from ginseng root extract by a thermostable β-glycosidase from Sulfolobussolfataricus. Bioscience Biotechnology and Biochemistry, 73, 316-321.

Park, S. J., Youn, S. Y., Ji, G. E., & Park, M. S. (2012).Whole cell biotransformation of major ginsenosides using Leuconostocs and Lactobacilli.Food Science and Biotechnology, 21, 839-844.

Park, S. Y., Bae, E. A., Sung, J. H., Lee, S. K., & Kim, D. H. (2001).Purification and characterization of ginsenoside Rb1-metabolizing β-glucosidase from Fusobacterium K-60, a human intestinal anaerobic bacterium.Bioscience Biotechnology and Biochemistry, 65, 1163-1169.

Quan, L. H., Kim, Y. J., Li, G. H., Choi, K. T., & Yang, D. C. (2013). Microbial transformation of ginsenoside Rb1 to compound K by Lactobacillus paralimentarius.World Journal of Microbiology and Biotechnology, 29, 1001-1007.

Quan, L. H., Liang, Z., Kim, H. B., Kim, S. H., Kim, S. Y., Noh, Y. D., et al. (2008). Conversion of ginsenoside Rd to compound K by crude enzymes extracted from Lactobacillus brevis LH8. Journal of Ginseng Research, 32, 226-231.

Quan, L. H., Min, J. W., Sathiyamoorthy, S., Yang, D. U., Kim, Y. J., & Yang, D. C. (2012). Biotransformation of ginsenosides Re and Rg1 into ginsenosides Rg2 and Rh1 by recombinant β-glucosidase.Biotechnology Letters, 34, 913-917.

Quan, L. H., Piao, J. Y., Min, J. W., Kim, H. B., Kim, S. R., Yang, D. U., et al. (2011). Biotransformation of ginsenoside Rb1 to prosapogenins, gypenoside XVII, ginsenoside Rd, ginsenoside F2, and compound K by Leuconostocmesenteroides DC102.Journal of Ginseng Research, 35, 344-351.

Quan, L. H., Piao, J. Y., Min, J. W., Yang, D. U., Lee, H. N., & Yang, D. C. (2011). Bioconversion of ginsenoside Rb1 into compound K by Leuconostoccitreum LH1 isolated from kimchi. Brazilian Journal of Microbiology, 42, 1227-1237.

Quan, L. H., Wang, C., Jin, Y., Wang, T. R., Kim, Y. J., & Yang, D. C. (2013).Isolation and characterization of novel ginsenoside-hydrolyzing glycosidase from Microbacteriumesteraromaticum that transforms ginsenoside Rb2 to rare ginsenoside 20(S)-Rg3. AntonieVan Leeuwenhoek, 104, 129-137.

Ruan, C. C., Zhang, H., Zhang, L. X., Liu, Z., Sun, G. Z., Lei, J., et al. (2009). Biotransformation of ginsenosideRf to Rh1 by recombinant β-glucosidase. Molecules, 14, 2043-2048.

Son, J. W., Kim, H. J., & Oh, D. K. (2008).Ginsenoside Rd production from the major ginsenoside Rb1 by β-glucosidase from Thermuscaldophilus.Biotechnology Letters, 30, 713-716.

Wang, L., Liu, Q. M., Sung, B. H., An, D. S., Lee, H. G., Kim, S. G., et al. (2011). Bioconversion of ginsenosides Rb1, Rb2, Rc and Rd by novel β-glucosidase hydrolyzing outer 3-O glycoside from Sphingomonas sp. 2F2: cloning, expression, and enzyme characterization. Journal of Biotechnology, 156, 125-133.

Yan, Q., Zhou, W., Shi, X., Zhou, P., Ju, D., & Feng, M. (2010).Biotransformation pathways of ginsenoside Rb1 to compound K by β-glucosidases in fungus PaecilomycesBainier sp. 229.Process Biochemistry, 45, 1550-1556.

Ye, L., Zhou, C. Q., Zhou, W., Zhou, P., Chen, D. F., Liu, X. H., et al. (2010).Biotransformationof ginsenoside Rb1 to ginsenoside Rd by highly substrate-tolerantPaecilomycesbainier 229-7.BioresourceTechnology, 101, 7872-7876.

Yi, E. J., Lee, J. M., Yi, T. H., Cho, S. C., Park, Y. J.,Kook, M. C. (2012). Biotransformation of ginsenoside by Lactobacillus brevis THK-D57 Isolated from kimchi.Journal ofTheKorean Society of Food Science and Nutrition,25, 629-636.