Effect of fermentation by Lactobacillus reuteri and Lactobacillus acidophilus on antioxidant activity of quinoa extract

مجله پژوهشهای علوم و صنایع غذایی ایران

Article 6, Volume 17, Issue 5 - Serial Number 71, November and December 2021, Pages 747-759   

Document Type: Research Article

DOI: 10.22067/ifstrj.v17i5.88370

Authors

Rana Tahmasbi; Mahta Mirzaei^* ; Mohammadreza Khani

Department of Food Science and Technology, Shahr-e-Qods Branch, Islamic Azad University, Tehran, Iran.

Abstract

Introduction: Fermented foods, probiotic, prebiotics, and symbiotic, are among the most important groups of functional food that have attracted the attention of researchers during the last years. Proteolytic activity of lactic acid bacteria can lead to the production of peptides in the fermented product. The produced peptides can exhibit different biological activities such as antioxidant, antihypertensive, etc. that are influenced by the type of protein source, type of bacteria, time and conditions of fermentation process. Fermentation of various cereals such as quinoa seeds with high sugar and protein content by lactic acid bacteria can lead to the production of antioxidant peptides and improving their nutritional properties.
 
Materials and Methods: In this study, the role of Lactobacillus reuteri and Lactobacillus acidophilus and the combination of two bacteria on the progress of fermentation and antioxidant activity of quinoa extract was investigated. The fermentation process was started by separate and simultaneous inoculating of Lactobacillus reuteri and Lactobacillus acidophilus and continued for 72 hours at 37° C. Sampling was performed every 24 hours of fermentation and samples were kept at -20° C for further analysis. The parameters such as pH, acidity, amount of soluble protein, degree of hydrolysis, amount of phenolic compounds and DPPH and ABTS radical scavenging activity were determined.
 
Results and Discussion: Lactobacillus acidophilus showed higher acidification capacity than Lactobacillus reuteri. The amount of acidity in the sample fermented by Lactobacillus acidophilus increased from 0.27 to 1.13 % after 72 hours, while this amount was measured as 0.80 % for sample fermented by Lactobacillus reuteri. The amount of soluble protein and the degree of hydrolysis increased in samples fermented by both species. However, the largest increase was related to the sample fermented by Lactobacillus reuteri, so that the amount of soluble protein increased from 0.72 to 0.88 mg / ml and the value of free amino groups increased from 20.28 to 58.14 µM leucin/ mg protein during 72 hours of fermentation. The DPPH and ABTS radical scavenging activity increased in all fermented samples. The highest antioxidant activity was observed in samples fermented by Lactobacillus reuteri, followed by a combination of two bacteria (50:50) and Lactobacillus acidophilus. The amounts of phenolic compounds increased in all fermented samples. However, the highest increase was related to the sample fermented by Lactobacillus reuteri, so that it increased from 0/73 to 16.21 mg Gallic acid / ml after 72 hours of fermentation. Therefore, the results showed that despite the higher acidifying power of Lactobacillus acidophilus in quinoa extract, but Lactobacillus reuteri exhibited higher proteolytic activity, more ability to produce antioxidant peptides and also release phenolic compounds during the fermentation process.Simultaneous use of the two bacteria did not intensify the proteolytic activity and antioxidant activity of peptides, and the greatest increase in acidity, proteolysis, and antioxidant activity occurred in the first 24 hours of fermentation. Fermented extracts showed higher ABTS radical inhibitory activity than DPPH radical inhibition, indicating the hydrophilic nature of most produced antioxidant compounds. The highest levels of antioxidant activity were observed in samples fermented by Lactobacillus reuteri, a combination of Lactobacillus reuteri and Lactobacillus acidophilus (50:50) and Lactobacillus acidophilus, respectively. The results showed that fermentation by Lactobacillus reutri has the greatest effect on the production of antioxidant peptides and the release of phenolic compounds. The results of this study confirm the effectiveness of fermentation methods on improving the healing properties of quinoa extract and Lactobacillus reuteri was a more effective bacterium in fermentation and production of antioxidant peptides compared to Lactobacillus acidophilus. Simultaneous use of two bacteria did not increase the intensity of fermentation and did not improve the antioxidant activity compared to single use of each bacteria. Finally, the results of this study showed that fermentation of quinoa extract improves its antioxidant properties and has the potential to be used as a fermented beverage.

Keywords

Antioxidant activity; Fermentation; Lactobacillus reuteri ; Lactobacillus acidophilus; Quinoa extract

References

Apostolidis, E., Kwon, Y.-I., Ghaedian, R., Shetty, K., 2007. Fermentation of milk and soymilk by Lactobacillus bulgaricus and Lactobacillus acidophilus enhances functionality for potential dietary management of hyperglycemia and hypertension. Food biotechnology 21, 217-236.

Abugoch, L., Castro, E., Tapia, C., Añón, M.C., Gajardo, P., Villarroel, A., 2009. Stability of quinoa flour proteins (Chenopodium quinoa Willd.) during storage. International journal of food science & technology 44, 2013-2020.

Akpinar-Bayizit, A., Yilmaz-Ersan, L., Ozcan, T., 2010. Determination of boza's organic acid composition as it is affected by raw material and fermentation. International Journal of Food Properties 13, 648-656.

Ankolekar, C., Pinto, M., Greene, D., Shetty, K., 2012. In vitro bioassay based screening of antihyperglycemia and antihypertensive activities of Lactobacillus acidophilus fermented pear juice. Innovative food science & emerging technologies 13, 221-230.

Afify, A.E.-M.M., El Baroty, G.S., El Baz, F.K., El Baky, H.H.A., Murad, S.A., 2018. Scenedesmus obliquus: Antioxidant and antiviral activity of proteins hydrolyzed by three enzymes. Journal of Genetic Engineering and Biotechnology 16, 399-408.

Bagheri F, Mirdamadi S, Mirzaei M, Safavid M. 1398. Production of beneficial fermented milk by lactobacilli isolated from traditional Iranian dairy products. Quarterly Journal of New Food Technologies, 2: 255-243.

Bianchi, F., Rossi, E., Gomes, R., Sivieri, K., 2015. Potentially synbiotic fermented beverage with aqueous extracts of quinoa (Chenopodium quinoa Willd) and soy. Food Science and Technology International 21, 403-415.

Chung, Y.-C., Chang, C.-T., Chao, W.-W., Lin, C.-F., Chou, S.-T., 2002. Antioxidative activity and safety of the 50 ethanolic extract from red bean fermented by Bacillus subtilis IMR-NK1. Journal of Agricultural and Food Chemistry 50, 2454-2458.

Chen, G.-W., Tsai, J.-S., Pan, B.S., 2007. Purification of angiotensin I-converting enzyme inhibitory peptides and antihypertensive effect of milk produced by protease-facilitated lactic fermentation. International Dairy Journal 17, 641-647.

Ceballos‐González, C., Bolívar‐Monsalve, J., Ramírez‐Toro, C., Bolívar, G.A., 2018. Effect of lactic acid fermentation on quinoa dough to prepare gluten‐free breads with high nutritional and sensory quality. Journal of Food Processing and Preservation 42, e13551.

Dallagnol, A.M., Pescuma, M., De Valdez, G.F., Rollán, G., 2013. Fermentation of quinoa and wheat slurries by Lactobacillus plantarum CRL 778: proteolytic activity. Applied microbiology and biotechnology 97, 3129-3140.

Ebrahimi Jam S., Zarrin Qalami S., Ganjloo A. 1398. Production of gluten-free fermented beverage based on quinoa by probiotic bacteria, Journal of Food Industry Research, 1: 42-27.

Fitznar, H.P., Lobbes, J.M., Kattner, G., 1999. Determination of enantiomeric amino acids with high-performance liquid chromatography and pre-column derivatisation with o-phthaldialdehyde and N-isobutyrylcysteine in seawater and fossil samples (mollusks). Journal of Chromatography A 832, 123-132.

Griffiths, M.W., Tellez, A.M., 2013. Lactobacillus helveticus: the proteolytic system. Frontiers in Microbiology 4, 30.

Izadi A., Zarrin Qalami S., Ganjloo A. 1396. Production of useful fermented beverage based on rice containing natural sweetener of honey. Journal of Food Science and Technology, Volume 62, Number 14, pp. 201-214.

Juanmardi A, Labafi M, Khodanian F, Salehi A. 1395. Feasibility Study of Fermented Beverage Extraction from Red Beet Extract by Lactic Acid Bacteria, Journal of Food Science and Technology 56: 9-1.

Juan, M.-Y., Chou, C.-C., 2010. Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food microbiology 27, 586-591.

Karbasi M., Mousavi M., Yarmand M. S. 1394. Production and packaging of fermented beverage from date juice containing Lactobacillus rhamnosus, Journal of Food Processing and Storage, 2: 38-17.

Khalili F, Erjaei Z. 1397. Effect of sourdough fermentation containing Lactobacillus plantarum and Lactobacillus ruteri on sensory, physicochemical and stale properties of barley bread. Journal of Food Science and Nutrition, 3: 42 -33.

Katina, K., Liukkonen, K.-H., Kaukovirta-Norja, A., Adlercreutz, H., Heinonen, S.-M., Lampi, A.-M., Pihlava, J.-M., Poutanen, K., 2007. Fermentation-induced changes in the nutritional value of native or germinated rye. Journal of Cereal Science 46, 348-355.

Kim, S.-K., 2013. Marine proteins and peptides: biological activities and applications. John Wiley & Sons.

Lowry, O., Rosebrough, N., Farr, A., Randall, R., 1951a. Total protein estimation by Lowry's method. J. Biol. Chem 193, 265.

Moayedi A, NikPayam M, Khomeiri M, Aghdaei S. 1396. Antibacterial activity of hydrolyzed proteins obtained from enzymatic digestion of soy protein isolates on some food index bacteria. Journal of Applied Microbiology in Food Industry, 3: 31-22.

Mizuno, S., Matsuura, K., Gotou, T., Nishimura, S., Kajimoto, O., Yabune, M., Kajimoto, Y., Yamamoto, N., 2005. Antihypertensive effect of casein hydrolysate in a placebo-controlled study in subjects with high-normal blood pressure and mild hypertension. British Journal of Nutrition 94, 84-91.

Magala, M., Kohajdova, Z., Karovičová, J., Greifova, M., Hojerova, J., 2015. Application of lactic acid bacteria for production of fermented beverages based on rice flour. Czech Journal of Food Sciences 33, 458-463.

Mirzaei, M., Mirdamadi, S., Ehsani, M.R., Aminlari, M., 2018. Production of antioxidant and ACE-inhibitory peptides from Kluyveromyces marxianus protein hydrolysates: Purification and molecular docking. Journal of Food and Drug Analysis 26, 696-705.

National Standard No. 11117. 1989. Fermented Milks - Kefir Drink - Characteristics and Test Methods.

Pérez-Escalante, E., Jaimez-Ordaz, J., Castañeda-Ovando, A., Contreras-López, E., Añorve-Morga, J., González-Olivares, L.G., 2018. Antithrombotic activity of milk protein hydrolysates by lactic acid bacteria isolated from commercial fermented milks. Brazilian Archives of Biology and Technology 61.

Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C., 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free radical biology and medicine 26, 1231-1237.

Rathore, S., Salmerón, I., Pandiella, S.S., 2012. Production of potentially probiotic beverages using single and mixed cereal substrates fermented with lactic acid bacteria cultures. Food Microbiology 30, 239-244.

Sade Miri S, Lari H, Arab A. 1394. Measurement of total anthocyanin phenol and antioxidant activity in pericarb of pumpkin fruit of Qazvini cultivar Cucurbita pepo L.var squash. National Conference on New Topics in Agriculture, 3: 275-267.

Souri A, Mirzaei M, Mirdamadi S. 1397. Evaluation of the antioxidant effect of green tea leaf extract on the survival of probiotic bacteria in watermelon juice. Journal of Food Science and Technology, 85: 86-73.

Sharma, N., Singh, N., Singh, O., Pandey, V., Verma, P., 2011. Oxidative stress and antioxidant status during transition period in dairy cows. Asian-Australasian Journal of Animal Sciences 24, 479-484.

Shobharani, P., Nanishankar, V., Halami, P., Sachindra, N., 2014. Antioxidant and anticoagulant activity of polyphenol and polysaccharides from fermented Sargassum sp. International journal of biological macromolecules 65, 542-548.

Saadi, S., Saari, N., Anwar, F., Hamid, A.A., Ghazali, H.M., 2015. Recent advances in food biopeptides: Production, biological functionalities and therapeutic applications. Biotechnology advances 33, 80-116.

Sezgin, A.C., Sanlier, N., 2019. A new generation plant for the conventional cuisine: quinoa (Chenopodium Quinoa Willd.). Trends in Food Science & Technology.

Wright, K., Pike, O., Fairbanks, D., Huber, C., 2002. Composition of Atriplex hortensis, sweet and bitter Chenopodium quinoa seeds. Journal of Food Science 67, 1383-1385.

Wang, Y.-C., Yu, R.-C., Chou, C.-C., 2006. Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria. Food microbiology 23, 128-135.

Wang, X., Yu, H., Xing, R., Chen, X., Liu, S., Li, P., 2017. Optimization of the extraction and stability of antioxidative peptides from mackerel (Pneumatophorus japonicus) protein. BioMed research international 2017.

Zannini, E., Jeske, S., Lynch, K.M., Arendt, E.K., 2018. Development of novel quinoa-based yoghurt fermented with dextran producer Weissella cibaria MG1. International journal of food microbiology 268, 19-26.