DOI QR코드

DOI QR Code

LAB Fermentation Improves Production of Bioactive Compounds and Antioxidant Activity of Withania somnifera Extract and Its Metabolic Signatures as Revealed by LC-MS/MS

  • Yu, Jinhui (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences) ;
  • Geng, Yun (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences) ;
  • Xia, Han (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences) ;
  • Ma, Deyuan (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences) ;
  • Liu, Chao (College of Life Science, Shandong Normal University) ;
  • Wu, Rina (College of Food Science, Shenyang Agricultural University) ;
  • Wu, Junrui (College of Food Science, Shenyang Agricultural University) ;
  • You, Shengbo (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences) ;
  • Bi, Yuping (Institute of Crop Germplasm Resources, Shandong Academy of Agricultural Sciences)
  • Received : 2021.11.10
  • Accepted : 2022.01.18
  • Published : 2022.04.28

Abstract

In this study we investigated the effect of lactic acid bacteria (LAB) fermentation on the ingredients and anti-oxidant activity of Withania somnifera extract. Four strains of LAB could proliferate normally in medium containing W. somnifera extract after the pH reached 3.1~3.5. LAB fermentation increased the content of alcohols and ketones, endowing the extract with the characteristic aroma of fermentation. Compared to the control, the DPPH and ABTS free radical scavenging rates in the fermented samples were significantly improved, ranging from 48.5% to 59.6% and 1.2% to 6.4%. The content of total phenols was significantly increased by 36.1% during the fermentation of mixed bacteria. Moreover, the original composition spectrum of the extract was significantly changed while the differentially accumulated metabolites (DAMs) were closely related to bile secretion, tryptophan metabolism and purine metabolism. Therefore, LAB fermentation can be used as a promising way to improve the flavor and bioactivity of the extracts of W. somnifera, making the ferments more attractive for use as functional food.

Keywords

Acknowledgement

This work is supported by the Earmarked Fund for Algae Innovation Team of Modern Agro-industry Technology Research System in Shandong Province of China (No. SDAIT-26), and the fund from Shandong Provincial Natural Science Foundation of China (No. ZR2020QC228).

References

  1. Rai M, Jogee PS, Agarkar G, Dos SC. 2016. Anticancer activities of Withania somnifera: current research, formulations, and future perspectives. Pharm. Biol. 54: 189-197. https://doi.org/10.3109/13880209.2015.1027778
  2. Barnes DA, Barlow R, Nigam PS, Owusu-Apenten R. 2016. Antioxidant, anticancer and antibacterial activity of Withania somnifera aqueous root extract. J. Adv. Biol. Biotechnol. 5: 1-6.
  3. Mukherjee PK, Banerjee S, Biswas S, Das B, Kar A, Katiyar CK. 2021. Withania somnifera (L.) Dunal - Modern perspectives of an ancient Rasayana from Ayurveda. J. Ethnopharmacol. 264: 113157. https://doi.org/10.1016/j.jep.2020.113157
  4. Kumar K, Dubey M, Agnihotri A, Bhadauria S, Bhagyawsant SS, Shrivastava A. 2011. Antibacterial and phytochemical analysis of Withania somnifera aqueous and alcoholic extracts. J. Pharm. Res. 4: 3421-3423.
  5. Bara JK, Soni R, Jaiswal S, Dr. Saksena P. 2016. Phytochemical study of the plant Withania somnifera against various diseases. IOSRJAVS 9: 109-112. https://doi.org/10.9790/2380-090802109112
  6. Khazal KF, Hill DL, Grubbs CJ. 2014. Effect of Withania somnifera root extract on spontaneous estrogen receptor-negative mammary cancer in MMTV/Neu mice. Anticancer Res. 34: 6327-6332.
  7. Kataria H, Gupta M, Lakhman S, Kaur G. 2015. Withania somnifera aqueous extract facilitates the expression and release of GnRH: In vitro and in vivo study. Neurochem. Int. 89: 111-119. https://doi.org/10.1016/j.neuint.2015.08.001
  8. Rabhi C, Arcile G, Cariel L, Lenoir C, Bignon J, Wdzieczak-Bakala J, et al. 2015. Antiangiogenic-like properties of fermented extracts of ayurvedic medicinal plants. J. Med. Food 18: 1065-1072. https://doi.org/10.1089/jmf.2014.0128
  9. Sood A, Mehrotra A, Dhawan DK, Sandhir R. 2018. Indian Ginseng (Withania somnifera) supplementation ameliorates oxidative stress and mitochondrial dysfunctions in experimental model of stroke. Metab. Brain Dis. 33: 1261-1274. https://doi.org/10.1007/s11011-018-0234-2
  10. Singh P, Guleri R, Singh V, Kaur G, Kataria H, Singh B, et al. 2015. Biotechnological interventions in Withania somnifera (L.) Dunal. Biotechnol. Genet. Eng. Rev. 31: 1-20. https://doi.org/10.1080/02648725.2015.1020467
  11. Manwar J, Mahadik K, Sathiyanarayanan L, Paradkar A, Patil S. 2013. Comparative antioxidant potential of Withania somnifera based herbal formulation prepared by traditional and non-traditional fermentation processes. Integr. Med. Res. 2: 56-61. https://doi.org/10.1016/j.imr.2013.04.002
  12. Stefanovic E, Fitzgerald G, McAuliffe O. 2017. Advances in the genomics and metabolomics of dairy lactobacilli: A review. Food Microbiol. 61: 33-49. https://doi.org/10.1016/j.fm.2016.08.009
  13. Lu Y, Tan X, Lv Y, Yang G, Chi Y, He Q. 2020. Physicochemical properties and microbial community dynamics during Chinese horse bean-chili-paste fermentation, revealed by culture-dependent and culture-independent approaches. Food Microbiol. 85: 103309. https://doi.org/10.1016/j.fm.2019.103309
  14. Park E, Garcia CV, Youn S, Park C, Lee S. 2019. Fortification of γ-aminobutyric acid and bioactive compounds in Cucurbita moschata by novel two-step fermentation using Bacillus subtilis and Lactobacillus plantarum. LWT 102: 22-29. https://doi.org/10.1016/j.lwt.2018.07.065
  15. Perera D, Soysa P, Wijeratne S. 2016. Polyphenols contribute to the antioxidant and antiproliferative activity of Phyllanthus debilis plant in-vitro. BMC Complement. Altern. Med. 16: 339. https://doi.org/10.1186/s12906-016-1324-5
  16. Wannenmacher J, Cotterchio C, Schlumberger M, Reuber V, Gastl M, Becker T. 2019. Technological influence on sensory stability and antioxidant activity of beers measured by ORAC and FRAP. J. Sci. Food Agric. 99: 6628-6637. https://doi.org/10.1002/jsfa.9979
  17. Yu J, Wang Y, Sun J, Bian F, Chen G, Zhang Y, et al. 2017. Antioxidant activity of alcohol aqueous extracts of Crypthecodinium cohnii and Schizochytrium sp. J. Zhejiang Univ-Sc. B. 9: 797-806. https://doi.org/10.1631/jzus.B0860008
  18. Yu JH, Ma DY, Qu SJ, Liu YP, Xia H, Bian F, et al. 2020. Effects of different probiotic combinations on the components and bioactivity of Spirulina. J. Basic Microb. 60: 543-557. https://doi.org/10.1002/jobm.201900699
  19. Wuyts S, Van Beeck W, Oerlemans E, Wittouck S, Claes I, De Boeck I, et al. 2018. Carrot juice fermentations as man-made microbial ecosystems dominated by lactic acid bacteria. Appl. Environ. Microbiol. 84: e00134-18.
  20. De Vuyst L & Leroy F. 2020. Functional role of yeasts, lactic acid bacteria and acetic acid bacteria in cocoa fermentation processes. FEMS. Microbiol. Rev. 44: 432-453. https://doi.org/10.1093/femsre/fuaa014
  21. Bader J, Mast-Gerlach E, Popovic MK, Bajpai R, Stahl U. 2010. Relevance of microbial coculture fermentations in biotechnology. J. Appl. Microbiol. 109: 371-387. https://doi.org/10.1111/j.1365-2672.2009.04659.x
  22. Shiferaw TN and Augustin MA. 2020. Fermentation for tailoring the technological and health related functionality of food products. Crit. Rev. Food Sci. Nutr. 60: 2887-2913. https://doi.org/10.1080/10408398.2019.1666250
  23. Dan T, Wang D, Wu S, Jin R, Ren W, Sun T. 2017. Profiles of volatile flavor compounds in milk fermented with different proportional combinations of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus. Molecules 22: 1633-1647. https://doi.org/10.3390/molecules22101633
  24. Cui S, Zhao N, Lu W, Zhao F, Zheng S, Wang W, et al. 2019. Effect of different Lactobacillus species on volatile and nonvolatile flavor compounds in juices fermentation. Food Sci. Nutr. 7: 2214-2223. https://doi.org/10.1002/fsn3.1010
  25. Yi C, Li Y, Zhu H, Liu Y, Quan K. 2021. Effect of Lactobacillus plantarum fermentation on the volatile flavors of mung beans. LWT 146: 111434. https://doi.org/10.1016/j.lwt.2021.111434
  26. Hassan W, Noreen H, Rehman S, Gul S, Kamal MA, Kamdem JP, et al. 2017. Oxidative stress and antioxidant potential of one hundred medicinal plants. Curr. Top. Med. Chem. 17: 1336-1370. https://doi.org/10.2174/1568026617666170102125648
  27. Ricci A, Cirlini M, Calani L, Bernini V, Neviani E, Del RD, et al. 2019. In vitro metabolism of elderberry juice polyphenols by lactic acid bacteria. Food Chem. 276: 692-699. https://doi.org/10.1016/j.foodchem.2018.10.046
  28. Li Z, Teng J, Lyu Y, Hu X, Zhao Y, Wang M. 2018. Enhanced antioxidant activity for apple juice fermented with Lactobacillus plantarum ATCC14917. Molecules 24: 51. https://doi.org/10.3390/molecules24010051
  29. Li T, Jiang T, Liu N, Wu C, Xu H, Lei H. 2021. Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria. Food Chem. 339: 127859. https://doi.org/10.1016/j.foodchem.2020.127859
  30. Gauglitz JM, Aceves CM, Aksenov AA, Aleti G, Almaliti J, Bouslimani A, et al. 2020. Untargeted mass spectrometry-based metabolomics approach unveils molecular changes in raw and processed foods and beverages. Food Chem. 302: 125290. https://doi.org/10.1016/j.foodchem.2019.125290
  31. Arief II, Afiyah DN, Wulandari Z, Budiman C. 2016. Physicochemical properties, fatty acid profiles, and sensory characteristics of fermented beef sausage by probiotics Lactobacillus plantarum IIA-2C12 or Lactobacillus acidophilus IIA-2B4. J. Food Sci. 81: M2761-M2769. https://doi.org/10.1111/1750-3841.13509
  32. Kroemer G and Zitvogel L. 2020. Inosine: novel microbiota-derived immunostimulatory metabolite. Cell Res. 30: 942-943. https://doi.org/10.1038/s41422-020-00417-1
  33. Prabu S, Sivakumar K, Swaminathan M, Rajamohan R. 2015. Preparation and characterization of host-guest system between inosine and beta-cyclodextrin through inclusion mode. Spectrochim. Acta A Mol. Biomol. Spectrosc. 147: 151-157. https://doi.org/10.1016/j.saa.2015.03.056
  34. Garg D, Singh M, Verma N, Monika. 2022. Review on recent advances in fabrication of enzymatic and chemical sensors for hypoxanthine. Food Chem. 375: 131839. https://doi.org/10.1016/j.foodchem.2021.131839
  35. Fitscha P, Rauscha F, Rogatti W, Peskar BA, O'Grady J, Sinzinger H. 1991. 13,14-dihydro-PGE1, an in-vivo metabolite of PGE1, decreases mitotic activity induced by corticosteroid administration. Eicosanoids 4: 231-233.