Skip to main content

Advertisement

Log in

Utilization of Saccharina japonica as a Solid-Fermented Substrate for the Production of Bioactive Ethanolic Extract

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Marine biomass, Saccharina japonica was fermented as a solid-fermented substrate by Monascus spp. for the production of bioactive ethanolic extract. The 2,2-diphenyl-1-picrylhydrazyl (DPPH), 2,2′-Azino-bis-3-ethylbenzthiazoline-6-sulfonic acid (ABTS), superoxide anion radical scavenging and DNA protection activities of ethanolic extracts obtained from S. japonica fermented by M. purpureus (SjMp) showed the highest activity followed by M. kaoliang fermented S. japonica (SjMk) and unfermented (SjU) extract at 10 mg/mL concentration. Kinetic analysis revealed that ethanolic extract of fermented S. japonica inhibited the α-amylase competitively but α-glucosidase displayed competitive inhibition at 10 mg/mL concentration and non-competitive inhibition at 1 mg/mL concentration. The Linewaver-Burk kinetics analysis revealed that ethanolic extract of SjMk showed significantly higher Km value (4.55 mg) than SjMP (2.74 mg) followed by SjU (0.35 mg) at 10 mg/mL concentrations in α-amylase inhibition. But incase of α-glucosidase inhibition, the Km value was maximum in ethanolic extract of SjMp (2.30 mg) with Vmax (0.29 mg/min) at 10 mg/mL concentrations. Both of the fermented and unfermented samples did not show toxic effect on Caco-2 cells. The amino acid compositional analysis showed that fermentation process changed free amino acids contents in ethanolic extract. Monascus-fermented ethanolic extract showed antibacterial activity on Aeromonas hydrophila and Staphylococcus aureus. So, Monascus spp. fermented S. japonica extract played an important role in prevention of free radicals formation and hyperglycemia which can be applied in biofunctional food formulation.

Graphical Abstract

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Holdt, S.L., Kraan, S.: Bioactive compounds in seaweed: functional food applications and legislation. J. Appl. Phycol. 23(3), 543–597 (2011)

    Google Scholar 

  2. Hamouda, R.A., Sherif, S.A., Ghareeb, M.M.: Bioethanol production by various hydrolysis and fermentation processes with micro and macro green algae. Waste Biomass Valori. 1–7 (2017). https://doi.org/10.1007/s12649-017-9936-7

  3. Chen, H., Zhou, D., Luo, G., Zhang, S., Chen, J.: Macroalgae for biofuels production: progress and perspectives. Renew. Sust. Energ. Rev. 47, 427–437 (2015)

    Google Scholar 

  4. General, T., Kim, H.J., Prasad, B., Ngo, H.T.A., Vadakedath, N., Cho, M.G.: Fungal utilization of a known and safe macroalga for pigment production using solid-state fermentation. J. Appl. Phycol. 26(3), 1547–1555 (2014)

    Google Scholar 

  5. Uchida, M., Kurushima, H., Ishihara, K., Murata, Y., Touhata, K., Ishida, N., Niwa, K., Araki, T.: Characterization of fermented seaweed sauce prepared from nori (Pyropia yezoensis). J. Biosci. Bioeng. 123(3), 327–332 (2017)

    Google Scholar 

  6. Guneratnam, A.J., Xia, A., Murphy, J.D.: Comparative study of single-and two-stage fermentation of the brown seaweed Laminaria digitata. Energ. Convers. Manage. 148, 405–412 (2017)

    Google Scholar 

  7. Cheng, J., Lee, S.K., Palaniyandi, S.A., Suh, J.W., Yang, S.H.: Effect of fermentation with Monascus pilosus on the antioxidant activities and phenolic acid contents of adzuki bean (Vigna angularis). J. Coastal Life Med. 3, 276–283 (2015)

    Google Scholar 

  8. Lin, Y.L., Wang, T.H., Lee, M.H., Su, N.W.: Biologically active components and nutraceuticals in the Monascus-fermented rice: a review. Appl. Microbiol. Biotechnol. 77(5), 965–973 (2008)

    Google Scholar 

  9. Pattanagul, P., Pinthong, R., Phianmongkhol, A., Leksawasdi, N.: Review of Angkak production (Monascus purpureus). Chiang Mai J. Sci. 34, 319–328 (2007)

    Google Scholar 

  10. Aniya, Y., Ohtani, I.I., Higa, T., Miyagi, C., Gibo, H., Shimabukuro, M., Nakanishi, H., Taira, J.: Dimerumic acid as an antioxidant of the mold, Monascus anka. Free Radical Bio. Med. 28(6), 999–1004 (2000)

    Google Scholar 

  11. Dhale, M.A., Divakar, S., Kumar, S.U., Vijayalakshmi, G.: Isolation and characterization of dihydromonacolin-MV from Monascus purpureus for antioxidant properties. Appl. Microbiol. Biot. 73, 1197–1202 (2007)

    Google Scholar 

  12. Chairote, E., Chairote, G., Lumyong, S.: Red yeast rice prepared from Thai glutinous rice and the antioxidant activities. Chiang Mai J. Sci. 36(1), 42–49 (2009)

    Google Scholar 

  13. Kongbangkerd, T., Tochampa, W., Chatdamrong, W., Kraboun, K.: Enhancement of antioxidant activity of monascal waxy corn by a 2-step fermentation. Inter. J. Food Sci. Technol. 49(7), 1707–1714 (2014)

    Google Scholar 

  14. Kraboun, K., Tochampa, W., Chatdamrong, W., Kongbangkerd, T.: Effect of monosodium glutamate and peptone on antioxidant activity of monascal waxy corn. Int. Food Res. J. 20(2), 623–631 (2013)

    Google Scholar 

  15. Huang, Q., Zhang, H., Xue, D.: Enhancement of antioxidant activity of Radix Puerariae and red yeast rice by mixed fermentation with Monascus purpureus. Food chem. 226, 89–94 (2017)

    Google Scholar 

  16. Verspohl, E.: Novel pharmacological approaches to the treatment of type 2 diabetes. Pharmacol. Rev. 64, 188–237 (2012)

    Google Scholar 

  17. Nugerahani, I., Sutedja, A.M., Srianta, I., Widharna, R.M., Marsono, Y.: In vivo evaluation of Monascus-fermented durian seed for antidiabetic and antihypercholesterol agent. Food Res. 1(3), 83–88 (2017)

    Google Scholar 

  18. Shi, Y.C., Liao, V.H.C., Pan, T.M.: Monascin from red mold dioscorea as a novel antidiabetic and antioxidative stress agent in rats and Caenorhabditis elegans. Free Radical Bio. Med. 52(1), 109–117 (2012)

    Google Scholar 

  19. Yoshikawa, M., Nishida, N., Shimoda, H., Takada, M., Kawahara, Y., Matsuda, H.: Polyphenol constituents from Salacia species: quantitative analysis of mangiferin with alpha-glucosidase and aldose reductase inhibitory activities. Yakugaku Zasshi. 121(5), 371–378 (2001)

    Google Scholar 

  20. McDougall, G.J., Shpiro, F., Dobson, P., Smith, P., Blake, A., Stewart, D.: Different polyphenolic components of soft fruits inhibit α-amylase and α-glucosidase. J. Agr. Food Chem. 53(7), 2760–2766 (2005)

    Google Scholar 

  21. Adefegha, S.A., Oboh, G.: In vitro inhibition activity of polyphenol-rich extracts from Syzygium aromaticum (L.) Merr. & Perry (Clove) buds against carbohydrate hydrolyzing enzymes linked to type 2 diabetes and Fe2+-induced lipid peroxidation in rat pancreas. Asian Pac. J. Trop. Biomed. 2(10), 774–781 (2012)

    Google Scholar 

  22. Hasim, A.D., Ismail, A.I., Faridah, D.N.: Antioxidant and α-Glucosidase inhibitory activity of formulated ethanol extract of red yeast rice and rice bran. J. Pharmacogn. Phytochem. 6(5), 1891–1893 (2017)

    Google Scholar 

  23. Rouzbehan, S., Moein, S., Homaei, A., Moein, M.R.: Kinetics of α-glucosidase inhibition by different fractions of three species of Labiatae extracts: a new diabetes treatment model. Pharm. Biol. 55(1), 1483–1488 (2017)

    Google Scholar 

  24. Ojinnaka, M.T., Ojimelukwe, P.C., Ezeama, C.F.: Effect of fermentation period on the organic acid and amino acid contents of Ogiri from castor oil bean seeds. Malaysian J. Microbiol. 9(3), 201–212 (2013)

    Google Scholar 

  25. Berlowska, J., Dudkiewicz-Kołodziejska, M., Pawlikowska, E., Pielech-Przybylska, K., Balcerek, M., Czysowska, A., Kregiel, D.: Utilization of post-fermentation yeasts for yeast extract production by autolysis: the effect of yeast strain and saponin from Quillaja saponaria. J. I. Brewing. 123(3), 396–401 (2017)

    Google Scholar 

  26. Lee, B.J., Kim, J.S., Kang, Y.M., Lim, J.H., Kim, Y.M., Lee, M.S., Jeong, M.H., Ahn, C.B., Je, J.Y.: Antioxidant activity and γ-aminobutyric acid (GABA) content in sea tangle fermented by Lactobacillus brevis BJ20 isolated from traditional fermented foods. Food Chem. 122(1), 271–276 (2010)

    Google Scholar 

  27. Kono, I., Himeno, K.: Antimicrobial activity of Monascus pilosus IFO 4520 against contaminant of koji. Biosci. Biotech. Bioch. 63(8), 1494–1496 (1999)

    Google Scholar 

  28. Ferdes, M., Ungureanu, C., Radu, N., Chirvase, A.A.: Antimicrobial effect of Monascus purpureus red rice against some bacterial and fungal strains. New Biotechnol. 25, 1 (2009)

    Google Scholar 

  29. Kim, C., Jung, H., Kim, Y.O., Shin, C.S.: Antimicrobial activities of amino acid derivatives of Monascus pigments. FEMS Microbiol Lett. 264(1), 117–124 (2006)

    Google Scholar 

  30. Vendruscolo, F., Tosin, I., Giachini, A.J., Schmidell, W., Ninow, J.L.: Antimicrobial activity of Monascus pigments produced in submerged fermentation. J. Food Process Pres. 38(4), 1860–1865 (2014)

    Google Scholar 

  31. Rasmussen, R.R., Rasmussen, P.H., Larsen, T.O., Bladt, T.T., Binderup, M.L.: In vitro cytotoxicity of fungi spoiling maize silage. Food Chem. Toxicol. 49(1), 31–44 (2011)

    Google Scholar 

  32. Sanjukta, S., Rai, A.K., Muhammed, A., Jeyaram, K., Talukdar, N.C.: Enhancement of antioxidant properties of two soybean varieties of Sikkim Himalayan region by proteolytic Bacillus subtilis fermentation. J. Functional Foods. 14, 650–658 (2015)

    Google Scholar 

  33. Suraiya, S., Lee, J.M., Cho, H.J., Jang, W.J., Kim, D.G., Kim, Y.O., Kong, I.S.: Monascus spp. fermented brown seaweeds extracts enhance bio-functional activities. Food Biosci. 21, 90–99 (2018)

    Google Scholar 

  34. Dudonné, S., Vitrac, X., Coutière, P., Woillez, M., Mérillon, J.M.: Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J. Agr. Food Chem. 57(5), 1768–1774 (2009)

    Google Scholar 

  35. Oyaizu, M.: Studies on products of browning reaction prepared from glucosamine. JPN. J. Nutr. 44, 307–315 (1986)

    Google Scholar 

  36. Xiao, Y., Xing, G., Rui, X., Li, W., Chen, X., Jiang, M., Dong, M.: Enhancement of the antioxidant capacity of chickpeas by solid state fermentation with Cordyceps militaris SN-18. J. Funct. Foods. 10, 210–222 (2014)

    Google Scholar 

  37. McCue, P.P., Shetty, K.: Inhibitory effects of rosmarinic acid extracts on porcine pancreatic amylase in vitro. Asia Pac. J. Clin. Nutr. 13(1), 101–106 (2004)

    Google Scholar 

  38. Adisakwattana, S., Chanathong, B.: Alpha-glucosidase inhibitory activity and lipid-lowering mechanisms of Moringa oleifera leaf extract. Eur. Rev. Med. Pharmacol. Sci. 15(7), 803–808 (2011)

    Google Scholar 

  39. Kazeem, M.I., Adamson, J.O., Ogunwande, I.A.: Modes of inhibition of α-amylase and α-glucosidase by aqueous extract of Morinda lucida Benth leaf. BioMed Res. Inter. 2013 (2013)

  40. Liang, C.H., Syu, J.L., Mau, J.L.: Antioxidant properties of solid-state fermented adlay and rice by Phellinus linteus. Food Chem. 116(4), 841–845 (2009)

    Google Scholar 

  41. Kuo, C.F., Chyau, C.C., Wang, T.S., Li, C.R., Hu, T.J.: Enhanced antioxidant and anti-inflammatory activities of Monascus pilosus fermented products by addition of turmeric to the medium. J. Agr. Food Chem. 57(23), 11397–11405 (2009)

    Google Scholar 

  42. Hur, S.J., Lee, S.Y., Kim, Y.C., Choi, I., Kim, G.B.: Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem. 160, 346–356 (2014)

    Google Scholar 

  43. Larios-Cruz, R., Buenrostro-Figueroa, J., Prado-Barragán, A., Rodríguez-Jasso, R.M., Rodríguez-Herrera, R., Montañez, J.C., Aguilar, C.N.: Valorization of grapefruit by-products as solid support for solid-state fermentation to produce antioxidant bioactive extracts. Waste Biomass Valori. 1–7 (2017). https://doi.org/10.1007/s12649-017-0156-y

  44. Farvin, K.S., Jacobsen, C.: Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food chem. 138(2–3), 1670–1681 (2013)

    Google Scholar 

  45. Chandrasekara, A., Shahidi, F.: Bioaccessibility and antioxidant potential of millet grain phenolics as affected by simulated in vitro digestion and microbial fermentation. J. Funct. Foods. 4, 226–237 (2012)

    Google Scholar 

  46. Ratner, R.E.: Controlling postprandial hyperglycemia. Am. J. Cardiol. 88(6), 26–31 (2001)

    Google Scholar 

  47. Kim, Y.M., Jeong, Y.K., Wang, M.H., Lee, W.Y., Rhee, H.I.: Inhibitory effect of pine extract on α-glucosidase activity and postprandial hyperglycemia. Nutrition. 21(6), 756–761 (2005)

    Google Scholar 

  48. Srianta, I., Kusumawati, N., Nugerahani, I., Artanti, N., Xu, G.R.: In vitro α-glucosidase inhibitory activity of Monascus-fermented durian seed extracts. Inter. Food Res. J. 20(2), 533–536 (2013)

    Google Scholar 

  49. Krishnasamy, G., Muthusamy, K.: In vitro evaluation of antioxidant and antidiabetic activities of Syzygium densiflorum fruits. Asian Pac. J. Tropical Dis. 5(11), 912–917 (2015)

    Google Scholar 

  50. Saravana, P.S., Choi, J.H., Park, Y.B., Woo, H.C., Chun, B.S.: Evaluation of the chemical composition of brown seaweed (Saccharina japonica) hydrolysate by pressurized hot water extraction. Algal Res. 13, 246–254 (2016)

    Google Scholar 

  51. Eom, S.H., Kang, Y.M., Park, J.H., Yu, D.U., Jeong, E.T., Lee, M.S., Kim, Y.M.: Enhancement of polyphenol content and antioxidant activity of brown alga Eisenia bicyclis extract by microbial fermentation. Fish. Aquat. Sci. 14(3), 192–197 (2011)

    Google Scholar 

  52. Meillisa, A., Siahaan, E.A., Park, J.N., Woo, H.C., Chun, B.S.: Effect of subcritical water hydrolysate in the brown seaweed Saccharina japonica as a potential antibacterial agent on food-borne pathogens. J. Appl. Phycol. 25(3), 763–769 (2013)

    Google Scholar 

  53. Fernandes, M.B., Gonçalves, J.E., Scotti, M.T., de Oliveira, A.A., Tavares, L.C., Storpirtis, S.: Caco-2 cells cytotoxicity of nifuroxazide derivatives with potential activity against Methicillin-resistant Staphylococcus aureus (MRSA). Toxicol. In Vitro. 26(3), 535–540 (2012)

    Google Scholar 

  54. Fernandes, M.D.R.V., Pfenning, L.H., Costa-Neto, C.M.D., Heinrich, T.A., Alencar, S.M.D., Lima, M.A.D., Ikegaki, M.: Biological activities of the fermentation extract of the endophytic fungus Alternaria alternata isolated from Coffea arabica L. Braz. J. Pharm. Sci. 45(4), 677–685 (2009)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to In-Soo Kong.

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 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suraiya, S., Park, H.D., Jang, W.J. et al. Utilization of Saccharina japonica as a Solid-Fermented Substrate for the Production of Bioactive Ethanolic Extract. Waste Biomass Valor 11, 1917–1928 (2020). https://doi.org/10.1007/s12649-018-0503-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-018-0503-7

Keywords