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Stimulatory Agents Simultaneously Improving the Production and Antioxidant Activity of Polyphenols from Inonotus obliquus by Submerged Fermentation

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Abstract

Polyphenols are important secondary metabolites from the edible and medicinal mushroom Inonotus obliquus. Both the rarity of I. obliquus fruit body and the low efficiency of current method of submerged fermentation lead to a low yield of polyphenols. This study was aimed to determine the effect of applying stimulatory agents to liquid cultured I. obliquus on the simultaneous accumulation of exo-polyphenols (EPC) and endo-polyphenols (IPC). Linoleic acid was the most effective out of the 17 tested stimulatory agents, the majority of which increased the EPC and IPC production. The result was totally different from the stimulatory effect of Tween 80 for polysaccharide production in previous studies. The addition of 1.0 g/L linoleic acid on day 0 resulted in 7-, 14-, and 10-fold of increase (p < 0.05) in the production of EPC extracted by ethyl acetate (EA-EPC), EPC extracted by n-butyl alcohol (NB-EPC), and IPC, and significantly increased the production of ferulic acid, gallic acid, epicatechin-3-gallate (ECG), epigallocatechin-3-gallate (EGCG), phelligridin G, inoscavin B, and davallialactone. The EA-EPC, BA-EPC, and IPC from the linoleic acid-containing medium had significantly (p < 0.05) stronger scavenging activity against 2,2-diphenyl-1-picrylhydrazyl radicals (DPPH), which was attributed to the higher content of these bioactive polyphenols.

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References

  1. Zhong, J. J., & Xiao, J. H. (2009). Secondary metabolites from higher fungi: discovery, bioactivity, and bioproduction. Advannces in Biochemical Engineering/Biotechnology, 113, 79–150.

    CAS  Google Scholar 

  2. Wasser, S. P. (2011). Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Applied Microbiology and Biotechnology, 89, 1323–1332.

    Article  CAS  Google Scholar 

  3. Nakajima, Y., Sato, Y., & Konishi, T. (2007). Antioxidant small phenolic ingredients in Inonotus obliquus (Persoon) Pilat (Chaga). Chemical and Pharmaceutical Bulletin, 55, 1222–1226.

    Article  CAS  Google Scholar 

  4. Hyun, K. J., Ha, W. C., Soon, S. H., Jeong, H. P., Jeongmi, L., & Sung, W. K. (2010). Effect of steam treatment on soluble phenolic content and antioxidant activity of the Chaga mushroom (Inonotus obliquus). Food Chemistry, 119, 619–625.

    Article  Google Scholar 

  5. Lee, I., Kim, Y., Jang, Y., Jung, J., & Yun, B. (2007). New antioxidant polyphenols from the medicinal mushroom Inonotus obliquus. Bioorganic and Medicinal Chemistry Letters, 17, 6678–6681.

    Article  CAS  Google Scholar 

  6. Cui, Y., Kim, D., & Park, K. (2005). Antioxidant effect of Inonotus obliquus. Journal of Ethnopharmacology, 96, 79–85.

    Article  Google Scholar 

  7. Kim, M., & Seguin, P. (2008). Phenolic compound concentration and antioxidant activities of Edible and Medicinal Mushrooms from Korea. Journal of Agricultural and Food Chemistry, 56, 7265–7270.

    Article  CAS  Google Scholar 

  8. Wasser, S. P., & Weis, A. L. (1999). Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: a modern perspective. Critical Reviews in Immunology, 19, 65–96.

    CAS  Google Scholar 

  9. Jang, H. G., Heo, B. G., Park, Y. S., Namiesnik, J., Barasch, D., Katrich, E., Vearasilp, K., Trakhtenberg, S., & Gorinstein, S. (2012). Chemical composition, antioxidant and anticancer effects of the seeds and leaves of indigo(Polygonum tinctorium Ait.) plant. Applied Biochemistry and Biotechnology, 167, 1986–2004.

    Article  CAS  Google Scholar 

  10. Zheng, W. F., Zhang, M. M., Zhao, Y. X., Wang, Y., Miao, K. J., & Wei, Z. W. (2009). Accumulation of antioxidant phenolic constituents in submerged cultures of Inonotus obliquus. Bioresource Technology, 100, 1327–1335.

    Article  CAS  Google Scholar 

  11. Zheng, W. F., Liu, Y. B., Pan, S. Y., Yuan, W. H., Dai, Y. C., & Wei, J. C. (2011). Involvements of S-nitrosylation and denitrosylation in the production of polyphenols by Inonotus obliquus. Applied Microbiology and Biotechnology, 90, 1763–1772.

    Article  CAS  Google Scholar 

  12. Xu, X. Q., & Zhu, J. W. (2011). Enhanced phenolic antioxidants production in submerged cultures of Inonotus obliquus in a ground corn stover medium. Biochemstry Engineering Journal, 58–59, 103–109.

    Article  Google Scholar 

  13. Zhu, L. H., & Xu, X. Q. (2013). Stimulatory effect of different Lignocellulosic materials for phenolic compound production and antioxidant activity from Inonotus obliquus in submerged fermentation. Applied Biochemistry and Biotechnology, 169, 2138–2152.

    Article  CAS  Google Scholar 

  14. Colon, M., & Nerin, C. (2012). Role of catechins in the antioxidant capacity of an active film containing green tea, green coffee, and grapefruit extracts. Journal of Agricultural and Food Chemistry, 60, 9842–9849.

    Article  CAS  Google Scholar 

  15. Lambert, J. D., & Elias, R. J. (2010). The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Archives Biochemistry and Biophysics, 501, 65–72.

    Article  CAS  Google Scholar 

  16. Singh, H. B., Singh, B. N., Singh, S. P., & Nautiyal, C. S. (2010). Solid-state cultivation of Trichoderma harzianum NBRI-1055 for modulating natural antioxidants in soybean seed matrix. Bioresource Technology, 64, 44–53.

    Google Scholar 

  17. Qian, M. S., Jing, J., Ye, M., Shaikh, F., Wang, H. Y., & Yang, L. (2014). Effect of nitric oxide on lachnumYMU50 extracellular polyphenol accumulation and antioxidant defense system. Applied Biochemistry and Biotechnology, 174, 1761–1770.

    Article  CAS  Google Scholar 

  18. Gassaraa, F., Ajila, C. M., Satinder, K. B., Verma, M., Tyagi, R. D., & Valero, J. R. (2012). Liquid state fermentation of apple pomace sludge for the production of ligninolytic enzymes and liberation of polyphenolic compounds. Process Biochemistry, 47, 999–1004.

    Article  Google Scholar 

  19. Chien, Y. L., Ho, C. T., Chiang, B. H., & Hwang, L. S. (2011). Effect of fermentation time on antioxidative activities of Ganoderma lucidum broth using leguminous plants as part of the liquid fermentation medium. Food Chemistry, 126, 1586–1592.

    Article  CAS  Google Scholar 

  20. Yang, F. C., Ke, Y. F., & Kuo, S. S. (2000). Effect of fatty acids on the mycelial growth and polysaccharide formation by Ganoderma lucidumin shake flask cultures. Enzyme and Microbial Technology, 27, 295–301.

    Article  CAS  Google Scholar 

  21. Park, J. P., Kim, S. W., & Hwang, H. J. (2002). Stimulatory effect of plant oils and fatty acids on the exo-biopolymer production in Cordyceps militaris. Enzyme and Microbial Technology, 31, 250–255.

    Article  CAS  Google Scholar 

  22. Lim, J. M., & Yun, J. W. (2006). Enhanced production of exopolysaccharides by supplementation of toluene in submerged culture of an edible mushroom Collybia maculata TG-1. Process Biochemistry, 41, 1620–1626.

    Article  CAS  Google Scholar 

  23. Hsieh, C., Wang, H., Chen, C. C., Hsu, T. H., & Tseng, M. H. (2008). Effect of plant oil and surfactant on the production of mycelial biomass and polysaccharides in submerged culture of Grifola frondosa. Biochemical Engineering Journal, 38, 198–205.

    Article  CAS  Google Scholar 

  24. Zhang, B. B., & Cheung, P. C. K. (2011). Use of stimulatory agents to enhance the production of bioactive exopolysaccharide from Pleurotus tuber-regium by submerged fermentation. Journal of Agricultural and Food Chemistry, 59, 1210–1216.

    Article  CAS  Google Scholar 

  25. Zhang, B. B., & Cheung, P. C. K. (2011). A mechanistic study of the enhancing effect of Tween 80 on the mycelial growth and exopolysaccharide production by Pleurotus tuber-regium. Bioresource Technology, 102, 8323–8326.

    Article  CAS  Google Scholar 

  26. Xu, X.Q., Quan, L.L., & Shen, M.W. (2015). Effect of chemicals on production, composition and antioxidant activity of polysaccharides of Inonotus obliquus. International Journal of Biological Macromolecules. Submitted.

  27. Leon, A. D., Garcia, B., Barba de la rosa, A. P., Villaseno, F., Estrada, A., & Lopez-revilla, R. (2003). Periplasmic penicillin G acylase activity in recombinant Escherichia coli cells permeabilized with organic solvents. Process Biochemistry, 39, 301–305.

    Article  Google Scholar 

  28. Chen, H., & Xu, X. Q. (2010). Optimization of hydroxyl radical scavenging activity of exopolysaccharides from Inonotus obliquus in submerged fermentation using response surface methodology. Journal of Microbiol and Biotechnology, 20, 835–843.

    CAS  Google Scholar 

  29. Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic phosphotunstic acid reagents. American Journal of Enology and Viticulture, 16, 144–158.

    CAS  Google Scholar 

  30. Hsieh, C., Tsai, M. J., Hsu, T. H., Chang, D. M., & Lo, C. T. (2005). Medium optimization for polysaccharide production of Cordyceps sinensis. Applied Microbiology and Biotechnology, 120, 145–157.

    CAS  Google Scholar 

  31. Xu, X. Q., Hu, Y., & Zhu, L. H. (2014). The capability of Inonotus obliquus for lignocellulosic biomass degradation in peanut shell and for simultaneous production of bioactive polysaccharides and polyphenols in submerged fermentation. Journal of the Taiwan Institute of Chemical Engineers, 45, 2851–2858.

    Article  CAS  Google Scholar 

  32. Ferri, M., Righetti, L., & Tassoni, A. (2011). Increasing sucrose concentrations promote phenylpropanoid biosynthesis in grapevine cell cultures. Journal of Plant Physiology, 168, 189–195.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the research grant from the Science and Technology Department of Zhejiang Province, China (2012C23075), and the National Natural Science Foundation of China.

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Correspondence to Xiangqun Xu.

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Xu, X., Shen, M. & Quan, L. Stimulatory Agents Simultaneously Improving the Production and Antioxidant Activity of Polyphenols from Inonotus obliquus by Submerged Fermentation. Appl Biochem Biotechnol 176, 1237–1250 (2015). https://doi.org/10.1007/s12010-015-1642-y

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  • DOI: https://doi.org/10.1007/s12010-015-1642-y

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