Abstract
Agro-industrial residues contain high nutritive value. Nowadays, various advanced researches have been done for the production of various value-added products, using these wastes as substrates in the fermentation media. Flaxseed, mustard, and rice bran meal, residues of oil industry, were used as substrates for fermentation. Submerged fermentation with soil-isolated fungal species of the genus Aspergillus sp. was done for oil production by using these substrates in the fermentation media. Effect of fermentation by the oleaginous species of Aspergillus on the nutritive value and functional properties of flaxseed, mustard, and rice bran meal has been discussed for the first time in the present study. After fermentation, the seed meals showed substantial increase in the protein and ash content. The fungal strains utilized the carbohydrate present in the seed meals for the production of highly nutritional metabolites, which decrease the sugar contents of the meals. The fungi also showed extracellular amylase and cellulase activities which helped to hydrolyze the carbohydrates present in these meals, to utilize them for their metabolism. The enhancement was also observed in terms of antioxidant activity of the meals. Increase in the total phenolic and flavonoid contents was observed after fermentation along with radical scavenging activity of 1,1-diphenyl-2-picrylhydrazyl and 2,2-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid reagents and ferric reduction potential. These effects of fermentation modify these cheap waste materials into nutrient dense substrates, which could be further used in the formulation of value-added products.
Similar content being viewed by others
Data Availability
The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code Availability
Not applicable.
References
Shirahigue, L. D., & Ceccato-Antonini, S. R. (2020). Agro-industrial wastes as sources of bioactive compounds for food and fermentation industries. Ciencia Rural, 50(4). https://doi.org/10.1590/0103-8478cr20190857
Stodolak, B., Starzyńska-Janiszewska, A., Wywrocka-Gurgul, A., & Wikiera, A. (2017). Solid-state fermented flaxseed oil cake of improved antioxidant capacity as potential food additive. Journal of Food Processing and Preservation, 41(2), 1–9. https://doi.org/10.1111/jfpp.12855
Panaite, T., Ropota, M., Turcu, R., Olteanu, M., Corbu, A. R., & Nour, V. (2017). Flaxseeds: Nutritional potential and bioactive com- pounds. Food Science and Technology Bulletin., 74, 65–73.
Swati, S. S., & Das, M. (2015). A brief overview: Present status on utilization of mustard oil and cake. Indian Journal of Traditional Knowledge, 14(2), 244–250.
dos Santos-Oliveira, M., Cipolatti, E. P., Furlong, E. B., & de Souza-Soares, L. (2012). Compostos fenólicos e atividade antioxidante em farelo de arroz (Oryza sativa) fermentado. Ciencia e Tecnologia de Alimentos, 32(3), 531–537. https://doi.org/10.1590/S0101-20612012005000071
Dua, A., Chander, S., Agrawal, S., & Mahajan, R. (2014). Antioxidants from defatted Indian Mustard (Brassica Juncea) protect biomolecules against in vitro oxidation. Physiology and Molecular Biology of Plants, 20(4), 539–543. https://doi.org/10.1007/s12298-014-0260-4
Nisa, K., Rosyida, V. T., Nurhayati, S., Indrianingsih, A. W., Darsih, C., & Apriyana, W. (2019). Total phenolic contents and antioxidant activity of rice bran fermented with lactic acid bacteria. IOP Conference Series: Earth and Environmental Science, 251(1). https://doi.org/10.1088/1755-1315/251/1/012020
Kamoun, O., Ayadi, I., Guerfali, M., Belghith, H., Gargouri, A., & Trigui-Lahiani, H. (2018). Fusarium verticillioides as a single-cell oil source for biodiesel production and dietary supplements. Process Safety and Environmental Protection, 118(June), 68–78. https://doi.org/10.1016/j.psep.2018.06.027
Khot, M., Gupta, R., Barve, K., Zinjarde, S., Govindwar, S., & RaviKumar, A. (2015). Fungal production of single cell oil using untreated copra cake and evaluation of its fuel properties for biodiesel. Journal of Microbiology and Biotechnology, 25(4), 459–463. https://doi.org/10.4014/jmb.1407.07074
Sugiharto, S., Isroli, I., Yudiarti, T., Widiastuti, E., Wahyuni, H. I., & Sartono, T. A. (2018). Effect of two-step fermentation by Chrysonilia crassa and Bacillus subtilis on nutritional values and antioxidative properties of agro-industrial by-products as poultry feed ingredients. Journal of Advanced Veterinary and Animal Research, 5(4), 472–480. https://doi.org/10.5455/javar.2018.e301
Nkhata, S. G., Ayua, E., Kamau, E. H., & Shingiro, J. B. (2018). Fermentation and germination improve nutritional value of cereals and legumes through activation of endogenous enzymes. Food Science and Nutrition, 6(8), 2446–2458. https://doi.org/10.1002/fsn3.846
Aliyah, A., Alamsyah, G., Ramadhani, R., & Hermansyah, H. (2017). Production of α-amylase and β-glucosidase from Aspergillus niger by solid state fermentation method on biomass waste substrates from rice husk, bagasse and corn cob. Energy Procedia, 136, 418–423.
Dhage, A. B., & Rathod, V. K. (2017). Intensification of β- glucosidase enzyme production from Aspergillus niger using ex- tractive fermentation with an aqueous two-phase system. Green Process Synthesis, 6, 441–445.
Zhai, S. S., Zhou, T., Li, M. M., Zhu, Y. W., Li, M. C., Feng, P. S., Zhang, X. F., Ye, H., Wang, W. C., & Yang, L. (2019). Fermentation of flaxseed cake increases its nutritional value and utilization in ducklings. Poultry Science, 98(11), 5636–5647. https://doi.org/10.3382/ps/pez326
Srivastava, R. K. (2018). Enhanced shelf life with improved food quality from fermentation processes. Journal of Food Technology and Preservation, 2(3), 1–7. http://www.alliedacademies.org/food-technology-and-preservation/
Monica, S. J., Joseph, M., & Iyer, P. (2016). A study on invitro antioxidant activity of fermented and unfermented flaxseed (Linum usitatissimum L). World Journal of Pharmaceutical Research, 5(4), 1720–1728. https://doi.org/10.20959/wjpr20164-5996
Miri, S., Hajihosseini, R., Saedi, H., Vaseghi, M., & Rasooli, A. (2019). Fermented soybean meal extract improves oxidative stress factors in the lung of inflammation/infection animal model. Annals of Microbiology, 69(13), 1507–1515. https://doi.org/10.1007/s13213-019-01534-y
Ma, J., Zhu, X., Shi, L., Ni, C., Hou, J., & Cheng, J. (2019). Enhancement of soluble protein, polypeptide production and functional properties of heat-denatured soybean meal by fermentation of Monascus purpureus 04093. CYTA - Journal of Food, 17(1), 1014–1022. https://doi.org/10.1080/19476337.2019.1695677
Shi, C., He, J., Yu, J., Yu, B., Huang, Z., Mao, X., Zheng, P., & Chen, D. (2015). Solid state fermentation of rapeseed cake with Aspergillus niger for degrading glucosinolates and upgrading nutritional value. Journal of Animal Science and Biotechnology, 6(1), 1–7. https://doi.org/10.1186/s40104-015-0015-2
Karimi, S., Soofiani, N. M., Mahboubi, A., & Taherzadeh, M. J. (2018). Use of organicwastes and industrial by-products to produce filamentous fungi with potential as aqua-feed ingredients. Sustainability (Switzerland), 10(9). https://doi.org/10.3390/su10093296
Mrudula, S., & Murugammal, R. (2011). Production of cellulase by Aspergillus niger under submerged and solid state fermentation using coir waste as a substrate. Brazilian Journal of Microbiology, 42(3), 1119–1127. https://doi.org/10.1590/S1517-83822011000300033
Thakur, M. S., Prapulla, S. G., & Karanth, N. G. (1988). Microscopic Observation of Sudan Black B Staining to Monitor Lipid Production by Microbes. Journal of Chemical Technology Biotechnology., 42, 129–134. https://doi.org/10.1002/jctb.280420206
McClenny, N. (2005). Laboratory detection and identification of Aspergillus species by microscopic observation and culture: The traditional approach. Medical Mycology, 43(SUPPL. 1), 125–128. https://doi.org/10.1080/13693780500052222
A.O.A.C. Official Methods of Analysis. 17th ed. of the association of official analytical chemists. Gaithersburg M D.USA. 2000.
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry. Physiol., 37(8), 911–917. https://doi.org/10.1139/o59-099
Bertrand, T. F., Frederic, T., & Robert, N. (2004). Production and partial characterization of a thermostable amylase from Ascomycetes yeast strain isolated from starchy soil (pp. 53–55). McGraw-Hill Inc.
Ghose, T. K. (1987). Measurement of caellulase activities. Pure and Applied Chemistry, 59(2), 257–268.
Singleton, V. L., Ortofehr, R., & Lamuela-Raventos, R. M. (1999). Analysis of total phenols and other oxidation substrate and antioxidants by means of Folin-Ciocalteau reagent. Methods in Enzymology, 299, 152–178.
Jagadish, L. K., Venkata Krishnan, V., Shenbhagaraman, R., & Kaviyarasan, V. (2009). Comparitive study on the antioxidant, anticancer and antimicrobial property of Agaricus bisporus (J. E. Lange) Imbach before and after boiling. African Journal of Biotechnology, 8, 654–661.
Yadav, M., Yadav, A., & Yadav, J. P. (2014). In vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana Lam. Asian Pacific Journal of Tropical Medicine, 7, S256–S261.
Adhikari, A., Darbar, S., Chatterjee, T., Das, M., et al. (2018). Spectroscopic studies on dual role of natural flavonoids in detoxification of lead poisoning: Bench-to-Bedside Preclinical Trial. ACS Omega, 3, 15975–15987. https://doi.org/10.1021/acsomega.8b02046
Miller, G. L. (1959). Use of Dinitrosalicylic acid reagent for the determination of reducing sugar. Analytical Chemistry., 31(3), 426–428. https://doi.org/10.1021/ac60147a030
Cai, C., Ma, J., Han, C., Jin, Y., Zhao, G., & He, X. (2019). Extraction and antioxidant activity of total triterpenoids in the mycelium of a medicinal fungus, Sanghuangporus sanghuang. Science and Reports, 9, 1–10.
Othman, A., Ismail, N., Ghani, A., & Adenan, I. (2007). Antioxidant capacity and phenolic content of cocoa beans. Food Chemistry, 100(4), 1523–1530.
Stodolak, B., Starzyńska-Janiszewska, A., & Mickowska, B. (2013). Effect of flaxseed oil-cake addition on the nutritional value of grass pea tempeh. Food Science & Technology Research, 19(6), 1107–1114.
Bandikari, R., Katike, U., Seelam, N. S., & Obulam, V. S. R. (2017). Valorization of de-oiled cakes for xylanase production and optimization using central composite design by Trichoderma koeningi isolate. Turkish Journal of Biochemistry., 42(3), 317–328. https://doi.org/10.1515/tjb-2016-0290
Kumari, N., Vinita, N. K., & Rani, P. (2018). Nutrient composition of full fat and defatted rice bran. Asian Journal of Dairy and Food Research, 37(1), 77–80. https://doi.org/10.18805/ajdfr.DR-1277
Muniraj, I. K., Xiao, L., Hu, Z., & Zhan, X. (2017). Screening and characterization of oleaginous fungi from Irish soil for growth under low carbon substrates. International Journal of Current Microbiology and Applied Sciences, 6(12), 772–781. https://doi.org/10.20546/ijcmas.2017.612.082
Jannathulla, R., Dayal, J. S., Ambasankar, K., & Muralidhar, M. (2017). Effect of fungal fermentation on the nutrient digestibility of guar meal in Penaeus vannamei. Indian Journal of Fisheries, 64(3), 67–74. https://doi.org/10.21077/ijf.2017.64.3.68434-10
Simwaka, J. E., Chamba, M. V. M., Huiming, Z., Masamba, K. G., & Luo, Y. (2017). Effect of fermentation on physicochemical and antinutritional factors of complementary foods from millet, sorghum, pumpkin and amaranth seed flours. International Food Research Journal, 24(5), 1869–1879.
Mukherjee, R., Chakraborty, R., & Dutta, A. (2016). Role of fermentation in improving nutritional quality of soybean meal - A review. Asian-Australasian Journal of Animal Sciences, 29(11), 1523–1529. https://doi.org/10.5713/ajas.15.0627
Yaşar, S., & Tosun, S. (2020). Improving nutritional qualities of tomato pomace by Pleurotusostreatus and Phanerochaetechrysosporium fermentation. KSU Journal of Agriculture and Nature, 23(2), 527–534. https://doi.org/10.18016/ksutarimdoga.vi.629347
Monga, M., Goyal, M., Kl, K., & Soni, G. (2011). Production and stabilization of amylases from Aspergillus niger. 129–134. http://mycosphere.org/pdfs/MC2_2_No3.pdf
Khan, J. A., & Kumar, Y. S. (2011). Production of alpha amylases by aspergillus niger using cheaper substrates employing solid state fermentation. International Journal of Plant, Animal and Environmental Sciencies, 1(3), 100–108.
Singh, A., Singh, N., & Bishnoi, N. R. (2009). Production of cellulases by Aspergillus heteromorphus from wheat straw under submerged fermentation. International Journal of Agricultural and Biosystems Engineering, 3(3), 124–127.
Cheng, J., Choi, B. K., Yang, S. H., & Suh, J. W. (2016). Effect of fermentation on the antioxidant activity of rice bran by monascus pilosus KCCM60084. Journal of Applied Biological Chemistry, 59(1), 57–62. https://doi.org/10.3839/jabc.2016.011
Park, S. Y., Jang, H. L., Lee, J. H., Choi, Y., Kim, H., Hwang, J., Seo, D., Kim, S., & Nam, J. S. (2017). Changes in the phenolic compounds and antioxidant activities of mustard leaf (Brassica juncea) kimchi extracts during different fermentation periods. Food Science and Biotechnology, 26(1), 105–112. https://doi.org/10.1007/s10068-017-0014-5
Sadh, P. K., Saharan, P., Duhan, S., & Duhan, J. S. (2017). Bio-enrichment of phenolics and antioxidant activity of combination of Oryza sativa and Lablab purpureus fermented with GRAS filamentous fungi. Resource-Efficient Technologies, 3(3), 347–352. https://doi.org/10.1016/j.reffit.2017.02.008
Acknowledgements
I sincerely thank and express my gratitude to IIEST, Shibpur, for supporting me throughout my work.
Author information
Authors and Affiliations
Contributions
Ruma Dutta: investigation, formal analysis, validation, writing original draft.
Saheli Ghosal: formal analysis, validation.
Dipak K. Bhattacharyya: conceptualization, methodology, supervision, writing—review and editing.
Jayati Bhowal: conceptualization, supervision, writing—review and editing.
Corresponding author
Ethics declarations
Ethics Approval
Not applicable.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dutta, R., Ghosal, S., Bhattacharyya, D.K. et al. Effect of Fungal Fermentation on Enhancement of Nutritional Value and Antioxidant Activity of Defatted Oilseed Meals. Appl Biochem Biotechnol 195, 2172–2195 (2023). https://doi.org/10.1007/s12010-022-04059-4
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-022-04059-4