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






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
Holdt, S.L., Kraan, S.: Bioactive compounds in seaweed: functional food applications and legislation. J. Appl. Phycol. 23(3), 543–597 (2011)
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
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)
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)
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)
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)
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)
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)
Pattanagul, P., Pinthong, R., Phianmongkhol, A., Leksawasdi, N.: Review of Angkak production (Monascus purpureus). Chiang Mai J. Sci. 34, 319–328 (2007)
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)
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)
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)
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)
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)
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)
Verspohl, E.: Novel pharmacological approaches to the treatment of type 2 diabetes. Pharmacol. Rev. 64, 188–237 (2012)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
Kono, I., Himeno, K.: Antimicrobial activity of Monascus pilosus IFO 4520 against contaminant of koji. Biosci. Biotech. Bioch. 63(8), 1494–1496 (1999)
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)
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)
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)
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)
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)
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)
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)
Oyaizu, M.: Studies on products of browning reaction prepared from glucosamine. JPN. J. Nutr. 44, 307–315 (1986)
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)
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)
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)
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)
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)
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)
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)
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
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)
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)
Ratner, R.E.: Controlling postprandial hyperglycemia. Am. J. Cardiol. 88(6), 26–31 (2001)
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)
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)
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)
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)
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)
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)
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)
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)
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declared no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-018-0503-7


