DOI QR코드

DOI QR Code

Metabolite profiling of fermented ginseng extracts by gas chromatography mass spectrometry

  • Received : 2016.09.07
  • Accepted : 2016.12.20
  • Published : 2018.01.15

Abstract

Background: Ginseng contains many small metabolites such as amino acids, fatty acids, carbohydrates, and ginsenosides. However, little is known about the relationships between microorganisms and metabolites during the entire ginseng fermentation process. We investigated metabolic changes during ginseng fermentation according to the inoculation of food-compatible microorganisms. Methods: Gas chromatography mass spectrometry (GC-MS) datasets coupled with the multivariate statistical method for the purpose of latent-information extraction and sample classification were used for the evaluation of ginseng fermentation. Four different starter cultures (Saccharomyces bayanus, Bacillus subtilis, Lactobacillus plantarum, and Leuconostoc mesenteroide) were used for the ginseng extract fermentation. Results: The principal component analysis score plot and heat map showed a clear separation between ginseng extracts fermented with S. bayanus and other strains. The highest levels of fructose, maltose, and galactose in the ginseng extracts were found in ginseng extracts fermented with B. subtilis. The levels of succinic acid and malic acid in the ginseng extract fermented with S. bayanus as well as the levels of lactic acid, malonic acid, and hydroxypruvic acid in the ginseng extract fermented with lactic acid bacteria (L. plantarum and L. mesenteroide) were the highest. In the results of taste features analysis using an electronic tongue, the ginseng extracts fermented with lactic acid bacteria were significantly distinguished from other groups by a high index of sour taste probably due to high lactic acid contents. Conclusion: These results suggest that a metabolomics approach based on GC-MS can be a useful tool to understand ginseng fermentation and evaluate the fermentative characteristics of starter cultures.

References

  1. Ye L, Zhou CQ, Zhou W, Zhou P, Chen DF, Liu XH, Shi XL, Feng MQ. Biotransformation of ginsenoside Rb1 to ginsenoside Rd by highly substratetolerant Paecilomyces bainier 229-7. Bioresource Technol 2010;101:7872-6. https://doi.org/10.1016/j.biortech.2010.04.102
  2. Mochizuki M, Yoo YC, Matsuzawa K, Sato K, Saiki I, Tonooka S, Samukawa K, Azuma I. Inhibitory effect of tumor metastasis in mice by saponins, ginsenoside-Rb2, 20 (R)-and 20 (S)-ginsenoside-Rg3, of red ginseng. Biol Pharm Bull 1995;18:1197-202. https://doi.org/10.1248/bpb.18.1197
  3. Lee SY, Jeong JJ, Eun SH, Kim DH. Anti-inflammatory effects of ginsenoside Rg1 and its metabolites ginsenoside Rh1 and 20 (S)-protopanaxatriol in mice with TNBS-induced colitis. Eur J Pharmacol 2015;762:333-43. https://doi.org/10.1016/j.ejphar.2015.06.011
  4. Zhang H, Li Z, Zhou Z, Yang H, Zhong Z, Lou C. Antidepressant-like effects of ginsenosides: a comparison of ginsenoside Rb 3 and its four deglycosylated derivatives, Rg 3, Rh 2, compound K, and 20 (S)-protopanaxadiol in mice models of despair. Pharmacol Biochem Behav 2016;140:17-26. https://doi.org/10.1016/j.pbb.2015.10.018
  5. Lee EJ, Song MJ, Kwon HS, Ji GE, Sung MK. Oral administration of fermented red ginseng suppressed ovalbumin-induced allergic responses in female BALB/c mice. Phytomedicine 2012;19:896-903. https://doi.org/10.1016/j.phymed.2012.04.008
  6. Kim HJ, Chae IG, Lee SG, Jeong HJ, Lee EJ, Lee IS. Effects of fermented red ginseng extracts on hyperglycemia in streptozotocin-induced diabetic rats. J Ginseng Res 2010;34:104-12. https://doi.org/10.5142/jgr.2010.34.2.104
  7. Kim BG, Choi SY, Kim MR, Suh HJ, Park HJ. Changes of ginsenosides in Korean red ginseng (Panax ginseng) fermented by Lactobacillus plantarum M1. Process Biochem 2010;45:1319-24. https://doi.org/10.1016/j.procbio.2010.04.026
  8. Xiang YZ, Shang HC, Gao XM, Zhang BL. A comparison of the ancient use of ginseng in traditional Chinese medicine with modern pharmacological experiments and clinical trials. Phytother Res 2008;22:851-8. https://doi.org/10.1002/ptr.2384
  9. Zhao H, Xu J, Ghebrezadik H, Hylands PJ. Metabolomic quality control of commercial Asian ginseng, and cultivated and wild American ginseng using 1 H NMR and multi-step PCA. J Pharm Biomed Anal 2015;114:113-20. https://doi.org/10.1016/j.jpba.2015.05.010
  10. Chen XP, Lin YP, Hu YZ, Liu CX, Lan K, Jia W. Phytochemistry, metabolism, and metabolomics of ginseng. Chin Herb Med 2015;7:98-108. https://doi.org/10.1016/S1674-6384(15)60026-0
  11. Yang SO, Shin YS, Hyun SH, Cho S, Bang KH, Lee D, Choi SP, Choi HK. NMRbased metabolic profiling and differentiation of ginseng roots according to cultivation ages. J Pharm Biomed Anal 2012;58:19-26. https://doi.org/10.1016/j.jpba.2011.09.016
  12. Mao Q, Bai M, Xu JD, Kong M, Zhu LY, Zhu H, Wang Q, Li SL. Discrimination of leaves of Panax ginseng and P. quinquefolius by ultra high performance liquid chromatography quadrupole/time-of-flight mass spectrometry based metabolomics approach. J Pharm Biomed Anal 2014;97:129-40. https://doi.org/10.1016/j.jpba.2014.04.032
  13. Pace R, Martinelli EM, Sardone N, Combarieu ED. Metabolomic evaluation of ginsenosides distribution in Panax genus (Panax ginseng and Panax quinquefolius) using multivariate statistical analysis. Fitoterapia 2015;101: 80-91. https://doi.org/10.1016/j.fitote.2014.12.013
  14. Kwon YK, Ahn MS, Park JS, Liu JR, In DS, Min BW, Kim SW. Discrimination of cultivation ages and cultivars of ginseng leaves using Fourier transform infrared spectroscopy combined with multivariate analysis. J Ginseng Res 2014;38:52-8. https://doi.org/10.1016/j.jgr.2013.11.006
  15. Park SE, Yoo SA, Seo SH, Lee KI, Na CS, Son HS. GC-MS based metabolomics approach of Kimchi for the understanding of Lactobacillus plantarum fermentation characteristics. LWT-Food Sci Technol 2016;68:313-21. https://doi.org/10.1016/j.lwt.2015.12.046
  16. Mastrangelo A, Ferrarini A, Rey-Stolle F, Garcia A, Barbas C. From sample treatment to biomarker discovery: a tutorial for untargeted metabolomics based on GC-(EI)-Q-MS. Anal Chim Acta 2015;900:21-35. https://doi.org/10.1016/j.aca.2015.10.001
  17. Paek IB, Moon W, Kim J, Ji HY, Kim SA, Sohn DH, Kim JB, Lee HS. Pharmacokinetics of a ginseng saponin metabolite compound K in rats. Biopharm Drug Dispos 2006;27:39-45. https://doi.org/10.1002/bdd.481
  18. Hsu BY, Lu TJ, Chen CH, Wang SJ, Hwang LS. Biotransformation of ginsenoside Rd in the ginseng extraction residue by fermentation with lingzhi (Ganoderma lucidum). Food Chem 2013;141:4186-93. https://doi.org/10.1016/j.foodchem.2013.06.134
  19. Chang CH, 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
  20. Jang M, Min JW, Yang DU, Jung SK, Kim SY, Yang DC. Ethanolic fermentation from red ginseng extract using Saccharomyces cerevisiae and Saccharomyces carlsbergensis. Food Sci Biotechnol 2011;20:131-5. https://doi.org/10.1007/s10068-011-0018-5
  21. Bonestroo MH, Kusters BJM, De Wit JC, Rombouts FM. Glucose and sucrose fermenting capacity of homofermentative lactic acid bacteria used as starters in fermented salads. Int J Microbiol 1992;15:365-76. https://doi.org/10.1016/0168-1605(92)90070-J
  22. Kim BG, Shin KS, Yoon TJ, Yu KW, Ra KS, Kim KM, Kim SY, Suh HJ. Fermentation of Korean red ginseng by Lactobacillus plantarum M-2 and its immunological activities. Appl Biochem Biotechnol 2011;65:1107-19.
  23. Kang BH, Lee KJ, Hur SS, Lee DS, Lee SH, Shin KS, Lee KS, Man J. Ginsenoside derivatives and quality characteristics of fermented ginseng using lactic acid bacteria. Korean J Food Preserv 2013;20:573-82. https://doi.org/10.11002/kjfp.2013.20.4.573
  24. Yan Z, Zheng XW, Chen JY, Han JS, Han BZ. Effect of different Bacillus strains on the profile of organic acids in a liquid culture of Daqu. J Inst Brew 2013;119: 78-83. https://doi.org/10.1002/jib.58
  25. Thoukis G, Ueda M, Wright D. The formation of succinic acid during alcoholic fermentation. Am J Enol Vitic 1995;16:1-8.
  26. Davis CR, Wibowo DJ, Lee TH, Fleet GH. Growth and metabolism of lactic acid bacteria during and after malolactic fermentation of wines at different pH. Appl Environ Microbiol 1986;51:539-45.
  27. Avenoza A, Busto JH, Canal N, Peregrina JM. Time course of the evolution of malic and lactic acids in the alcoholic and malolactic fermentation of grape must by quantitative 1H NMR (qHNMR) spectroscopy. J Agric Food Chem 2006;54:4715-20. https://doi.org/10.1021/jf060778p
  28. Park SJ, Kim DH, Paek NS, Kim SS. Preparation and quality characteristics of the fermentation product of ginseng by lactic acid bacteria (FGL). J Ginseng Res 2006;30:88-94. https://doi.org/10.5142/JGR.2006.30.2.088
  29. Cao J, Barbosa JM, Singh N, Locy RD. GABA transaminases from Saccharomyces cerevisiae and Arabidopsis thaliana complement function in cytosol and mitochondria. Yeast 2013;30:279-89. https://doi.org/10.1002/yea.2962
  30. Wang Z, Zhuge J, Fang H, Prior BA. Glycerol production by microbial fermentation: a review. Biotechnol Adv 2001;19:201-23. https://doi.org/10.1016/S0734-9750(01)00060-X
  31. Tahara Y, Toko K. Electronic tongues-A review. IEEE Sens J 2013;13: 3001-11. https://doi.org/10.1109/JSEN.2013.2263125
  32. Arrieta AA, Rodriguez-Mendez ML, De Saja JA, Blanco CA, Nimubona D. Prediction of bitterness and alcoholic strength in beer using an electronic tongue. Food Chem 2010;123:642-6. https://doi.org/10.1016/j.foodchem.2010.05.006
  33. Kang BS, Lee JE, Park HJ. Electronic tongue-based discrimination of Korean rice wines (makgeolli) including prediction of sensory evaluation and instrumental measurements. Food Chem 2014;151:317-23. https://doi.org/10.1016/j.foodchem.2013.11.084
  34. Kim N, Park KR, Park IS, Cho YJ, Bae YM. Application of a taste evaluation system to the monitoring of Kimchi fermentation. Biosens Bioelectron 2005;20:2283-91. https://doi.org/10.1016/j.bios.2004.10.007