Skip to main content
SpringerLink
Log in

Evaluation of antioxidant and antibacterial activities of the stems of Flammulina velutipes and Hypsizygus tessellatus (white and brown var.) extracted with different solvents

  • Original Paper
  • Published:
Journal of Food Measurement and Characterization Aims and scope Submit manuscript

Abstract

Mushrooms are rich in pharmacologically-important phytochemicals with reported medicinal values. In this study, the antibacterial activity of Flammulina velutipes (Enoki), Hypsizygus tessellatus (brown (Buna shimeji) and white (Bunapi shimeji) variants) stem extracts prepared with different solvents (water, methanol, acetone, and ethyl acetate) was investigated against Escherichia coli (E. coli ATCC 25922), Serratia marscenscens (S. marscenscens ATCC14756), Bacillus subtilis (B. subtilis ATCC 23857), and Staphylococcus aureus (S. aureus ATCC 25923). Their antioxidant activities were evaluated using radical scavenging assays of 1,1-diphenyl-2-picrylhydrazyl (DPPH), hydrogen peroxide (H2O2) and ferric reducing power (FRP). The water extracts of Enoki, Buna shimeji, and Bunapi shimeji showed bacterial growth inhibition in a concentration-dependent manner. From the obtained results, all the Enoki extracts showed a significant inhibition of the gram positive bacterial species (E. coli and S. marcescens > 68%) and a reduced inhibition of the gram negative bacterial species (B. subtilis and S. aureus < 45%, p < 0.05) after 24 h of incubation, while water extracts of Buna shimeji showed a significantly lower bacterial growth inhibition (< 60%) against all the studied bacteria. Bunapi shimeji extract inhibited S. marscenscens, E. coli, B. subtilis, and S. aureus by 54, 67, 46, and 44%, respectively. Methanol, acetone and ethyl acetate extracts showed significantly lower antibacterial activities (p < 0.05) compared to water extracts. Similarly, water extracts of Enoki, Bunapi shimeji and Buna shimeji showed significant antioxidant activities using DPPH (67.37 ± 0.01, 66.30 ± 0.18 and 42.44 ± 0.18%, respectively), hydrogen peroxide (67.87 ± 0.000, 45.52 ± 0.160 and 52.08 ± 0.000% respectively), and FRP (0.891 ± 0.001, 0.413 ± 0.001 and 0.491 ± 0.001, respectively) at the concentration of 1 mg/mL, compared to their respective methanol, acetone and ethyl acetate fractions. Upon LC-MS analysis of the most potent fraction (Enoki water extract), several phenolic compounds were identified, of which chromogenic acid, Methyl-5-O-caffeoylquinate, Kukoamine A, Kushenol K, Methyl Kushenol C, Glabrol, Sanggenon J, Corylin, and Moracenin C were confirmed. The antioxidant activities of the water extracts of Enoki, Buna shimeji and Bunapi shimeji correlated with their total phenolic and flavonoid contents, which were (166.56 ± 1.50, 108.13 ± 0.32 and 116.71 ± 0.01 µg gallic acid equivalent (GAE)/mg, respectively) and (96.33 ± 0.03, 82.18 ± 0.20 and 91.37 ± 0.15 µg quercetin equivalent (QE)/mg, respectively). Collectively, the study results have shown the studied mushrooms as potential natural sources of pharmacological agents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. K. Albouchi, F. Hassen, I. Casabianca, H. Hosni, S. Afr. J. Bot. 87, 164–174 (2013)

    Article  CAS  Google Scholar 

  2. G. Nevcihan, S. Cengiz, Food Sci. Biotechnol. 19(3), 691–696 (2010)

    Article  CAS  Google Scholar 

  3. S. Chatterjee, Z. Niaz, S. Gautam, V. Adhikari, A.P.S. Sharma, Food Chem. 101, 515–523 (2007)

    Article  CAS  Google Scholar 

  4. S.A.B.E. Van Acker, D.D. Berg, M.N.J.L. Tromp, D.H. Griffioen, W.P. Van Bennekom, W.J.F. Van Der Vijgh, A. Bast, Free Radic. Biol. Med. 20(3), 331–342 (1996)

    Article  PubMed  Google Scholar 

  5. P.G. Pietta, J. Nat. Prod. 63(7), 1035–1042 (2000)

    Article  CAS  PubMed  Google Scholar 

  6. M. Kosanić, B. Ranković, T. Stanojković, Saudi J. Biol. Sci. 22(4), 390–397 (2015)

    Article  CAS  PubMed  Google Scholar 

  7. L.R.B. Mariutti, G.P. de Mattos Barreto, N. Bragagnolo, A.Z. Mercadante, Braz. Arch. Biol. Technol. 51(6), 1225–1232 (2008)

    Article  Google Scholar 

  8. A.C. Kharkwal, H. Joshi, D.D. Panthari, P. Pant, M.K. Kharkwal, Asian J. Pharm. Clin. Res. 5(suppl 4), 1–4 (2012)

    Google Scholar 

  9. P. Manzi, A. Aguzzi, L. Pizzoferrato, Food Chem. 73, 321–325 (2001)

    Article  CAS  Google Scholar 

  10. P. Mattila, K. Konko, M. Eurola, J. Pihlava, J. Astola, L. Vahteristo, J. Agric. Food Chem. 49, 2343–2348 (2001)

    Article  CAS  PubMed  Google Scholar 

  11. A.M. Salem, T.A. Ibrahim, Int. J. Health Sci. 5, 6–8 (2011)

    Google Scholar 

  12. M.M. Omar, H.H. Shiekh, H.M. Gumgumjee, N.M. El-Kazanm, A.M. El-Gendy, Afr. J. Biotechnol. 11(71), 13576–13585 (2012)

    Google Scholar 

  13. G. Sundaram, M. Patra, S. Maniarasu, Zhong Xi Yi Jie He Xue Bao 10, 430–435 (2012)

    Article  PubMed  Google Scholar 

  14. D. Kolanjinathan, K. Stella, Int. J. Pharm. Biol. Arch. 2, 1738–1744 (2011)

    Google Scholar 

  15. X. Kim, S.K. Thomas, N.V. Li, Adv. Food Nutr. Res. 64, 213–224 (2011)

    Article  CAS  PubMed  Google Scholar 

  16. S. Ostrovidov, P. Franck, D. Joseph, L. Martarello, G. Kirsch, F. Belleville, P. Nabet, B. Dousset, J. Med. Chem. 43(9), 1762–1769 (2000)

    Article  CAS  PubMed  Google Scholar 

  17. B. Halliwell, Annu. Rev. Nutr. 16, 33–50 (1997)

    Article  Google Scholar 

  18. T. Nakayama, M. Yamada, T. Osawa, S. Kawakishi, Biochem. Pharmacol. 45(1), 265–267 (1993)

    Article  CAS  PubMed  Google Scholar 

  19. N. Gursoy, C. Sarikurkcu, B. Tepe, Food Sci. Biotchnol. 19(3), 691–696 (2010)

    Article  CAS  Google Scholar 

  20. S.R. Policegoudra, R.H. Chandrashekhar, S.M. Aradhya, L. Singh, Food Technol. Biotechnol. 49(2), 162–168 (2011)

    Google Scholar 

  21. K. Khandelwal, Practical Pharmacognosy: Techniques and Experiments, 19th edn. (Nirali Prakashan, Pune, 2008)

    Google Scholar 

  22. H. Usman, F. Abdulrahman, A. Usman, Afr. J. Tradit. Complement. Altern. Med. 6(3), 289–295 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. S. Saul, S. Wilen, Anal. Chem. 24(6), 979–983 (1952)

    Article  Google Scholar 

  24. D. Sruthi, Z. John, Int. food Res. J. 24(1), 75–85 (2017)

    CAS  Google Scholar 

  25. S. Mohammed, I. Auwal, S. Sanni, A. Ismail, A. Kyari, S. Abdullahi, I. Amina, Vet. Res. Forum. 5(2), 95–100 (2014)

    Google Scholar 

  26. K. Slinkard, V.L. Singleton, Am. J. Enol. Vitic. 28, 49–55 (1997)

    Google Scholar 

  27. A. Meda, C.E. Lamien, M. Romito, J. Millogo, O.G. Nacoulma, Food Chem. 91(3), 571–577 (2005)

    Article  CAS  Google Scholar 

  28. H.J.D. Dorman, O. Bachmayer, M. Kosar, R. Hiltunen, J. Agric. Food Chem. 52(4), 762–770 (2004)

    Article  CAS  PubMed  Google Scholar 

  29. M. Vijayalakshmi, K. Ruckmani, Bangladesh J. Pharmacol. 11(3), 570–572 (2016)

    Article  Google Scholar 

  30. O.O. Ogwuche, C.E. Elemike, E.E. Elemike, G. Obi, Clin. Phytosci. (2017). https://doi.org/10.1186/s40816-016-0027-2

    Article  Google Scholar 

  31. H.A. Hamid, R. Mutazah, M.M. Yusoff, N.A.A. Karim, A.F.A. Razis, Toxicology 108(Part B), 451–457 (2016)

    Google Scholar 

  32. S. Visht, S. Chaturvedi, Curr. Pharm. Res. 2(3), 584–599 (2012)

    Google Scholar 

  33. S.A. Addai, Z.R. Abdullah, A. Mutalib, Z.R. Addai, A. Abdullah, S.A. Mutalib, J. Med. Plants Res. 7(47), 3354–3359 (2013)

    CAS  Google Scholar 

  34. A. Ghasemzadeh, H.Z.E. Jaafar, A. Rahmat, J. Med. Plants Res. 5(7), 1147–1154 (2011)

    CAS  Google Scholar 

  35. B.N. Dar, S. Sharma, G.A. Nayik, Food Meas. 10(4), 755–761 (2016)

    Article  Google Scholar 

  36. M.A. Khan, M. Rahman, M.N. Sardar, M.S.I. Arman, M. Badrullslam, M.J.A. Khandakar, M. Rashid, G. Sadik, A.H.M.K. Alam, Asian Pac. J. Trop. Biomed. 6(5), 410–417 (2016)

    Article  Google Scholar 

  37. K. Liu, X. Xiao, J. Wang, C.Y.O. Chen, H. Hu, LWT Food Sci. Technol. 82, 154–161 (2017)

    Article  CAS  Google Scholar 

  38. J.B. Harborne, C.A. Williams, Phytochemistry 55(6), 481–504 (2000)

    Article  CAS  PubMed  Google Scholar 

  39. L.L. Bennett, S. Rojas, T. Seefeldt, J. Exp. Clin. Med. 4(4), 215–222 (2012)

    Article  CAS  Google Scholar 

  40. K. Jomova, M. Valko, Toxicology 283(2–3), 65–87 (2011)

    Article  CAS  PubMed  Google Scholar 

  41. S. Prasad, K. Phromno, V.R. Yadav, M.M. Chaturved, B.B. Aggarwal, Planta Med. 76(11), 1044–1063 (2010)

    Article  CAS  PubMed  Google Scholar 

  42. A. Cassidy, T. Huang, M.S. Rice, E.B. Rimm, S.S. Tworoger, Am. J. Clin. Nutr. (2014). https://doi.org/10.3945/ajcn.114.088708

    Article  PubMed  PubMed Central  Google Scholar 

  43. Y. Shen, L. Jin, P. Xiao, Y. Lu, J. Bao, J. Cereal. Sci. 49(1), 106–111 (2009)

    Article  CAS  Google Scholar 

  44. M.N. Alam, N.J. Bristi, M. Rafiquzzaman, Saudi Pharm. J. 21(2), 143–152 (2013)

    Article  PubMed  Google Scholar 

  45. M.H. Baratzadeh, A. Asoodeh, J. Chamani, Int. J. Food Sci. Technol. 48(8), 1603–1609 (2013)

    Article  CAS  Google Scholar 

  46. M.F. Maskam, J. Mohamad, M.A. Abdulla, A. Afzan, I. Wasiman, Sains Malays. 43(11), 1673–1684 (2014)

    CAS  Google Scholar 

  47. Z. Sroka, W. Cisowski, Food Chem. Toxicol. 41(6), 753–758 (2003)

    Article  CAS  PubMed  Google Scholar 

  48. P. Siddhuraju, K. Becker, J. Agric. Food Chem. 51(8), 2144–2155 (2003)

    Article  CAS  PubMed  Google Scholar 

  49. B.S.F. Bazzaz, M.H. Khayat, S.A. Emami, J. Asili, A. Sahebkara, E.J. Neishabory, Sci. Asia 37, 327–334 (2011)

    Article  CAS  Google Scholar 

  50. Z. Hodzic, H. Pasalic, A. Memisevic, M. Scrabovic, M. Saletovic, M. Poljakovic, Eur. J. Sci. Res. 28(3), 471–477 (2009)

    Google Scholar 

  51. F.Q. Schafer, G.R. Buettner, Free Radic. Biol. Med. 30(11), 1191–1212 (2001)

    Article  CAS  PubMed  Google Scholar 

  52. A. Moure, D. Franco, J. Sineiro, H. Domĭngguez, M.J. Nūňez, J.M. Lema, Food Res. Int. 34(2–3), 103–109 (2001)

    Article  CAS  Google Scholar 

  53. S. Kumari, S.K.C. Chang, J. Food Sci. 81(7), C1679–C1691 (2016)

    Article  CAS  PubMed  Google Scholar 

  54. K.J. Wang, Y.J. Zhang, C.R. Yang, J. Ethnopharmacol. 96(3), 483–487 (2005)

    Article  CAS  PubMed  Google Scholar 

  55. D.P.D. Hadjipavlou-Litina, T. Garnelis, C.M. Athanassopoulos, J. Enzyme Inhib. Med. Chem. 24(5), 1188–1193 (2009)

    Article  CAS  PubMed  Google Scholar 

  56. X.Q. Wang, H. Li, Z. Sun, L. Dong, L. Gao, C. Liu, Sci. Rep. (2016). https://doi.org/10.1038/srep36543

    Article  PubMed  PubMed Central  Google Scholar 

  57. X.H.X. He, J. Fang, L. Huang, J. Wang, J. Ethnopharmacol. 172, 10–29 (2015)

    Article  CAS  PubMed  Google Scholar 

  58. S.F.L.J. Wu, T. Miyase, A. Ueno, M. Kuroyanagi, T. Noro, Chem. Pharm. Bull. 33, 3231–3236 (1985)

    Article  CAS  Google Scholar 

  59. J.M.R. Ulrike Grienke, M. Richter, E. Walther, A. Hoffmann, J. Kirchmair, V. Makarov, S. Nietzsche, M. Schmidtke, Sci. Rep. (2016). https://doi.org/10.1038/srep27156

    Article  PubMed  PubMed Central  Google Scholar 

  60. E.W.C. Chan, Y.Y. Lim, M. Omar, Food Chem. 104(4), 1586–1593 (2007)

    Article  CAS  Google Scholar 

  61. C. Ramesh, M.G. Pattar, Pharmacogn. Res. 2(2), 107–112 (2010)

    Article  CAS  Google Scholar 

  62. H.J.D. Dorman, S.G. Deans, J. Appl. Microbiol. 88(2), 308–316 (2000)

    Article  CAS  PubMed  Google Scholar 

  63. M. Kosanic, B. Rankovic, T. Stanojkovic, J. Food Sci. 77(1), T20–T25 (2012)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support of Universiti Malaysia Pahang.

Author information

Authors and Affiliations

  1. Faculty of Industrial Science and Technology, Universiti Malaysia Pahang, Lebuhraya Tun Razak, 26300, Gambang, Pahang, Malaysia

    S. R. Shah, C. I. Ukaegbu & H. A. Hamid

  2. Faculty of Chemical Engineering and Natural Resources, Universiti Malaysia Pahang, Lebuhraya Tun Razak, 26300, Gambang, Pahang, Malaysia

    O. R. Alara

Authors
  1. S. R. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. I. Ukaegbu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. A. Hamid
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. R. Alara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. R. Shah.

Ethics declarations

Conflict of interest

The authors declared no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 388 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shah, S.R., Ukaegbu, C.I., Hamid, H.A. et al. Evaluation of antioxidant and antibacterial activities of the stems of Flammulina velutipes and Hypsizygus tessellatus (white and brown var.) extracted with different solvents. Food Measure 12, 1947–1961 (2018). https://doi.org/10.1007/s11694-018-9810-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11694-018-9810-8

Keywords

Search

Navigation