Abstract
Gamma-aminobutyric acid (GABA) is an active bio-compound with versatile physiological functions and, therefore, considerable attention is given to developing GABA-enriched functional foods. In this study, central composite design was used to optimize the fermentation conditions to obtain the highest GABA yield by Lactobacillus brevis. The optimal conditions of GABA production (1473.44 ppm) included 5% soy protein isolate, 3% inulin, and 96 h fermenting time at 37 °C. GABA-rich fermented solution (GABA-EFS) under optimal conditions had an appropriate emulsifying activity and water/oil holding capacity. Also, the reducing power assay revealed that GABA-EFS has electron donor groups with the ability to terminate the free radical chain reactions. Minimum inhibitory concentration results showed that Candida albicans was the most sensitive microorganism; whilst, Staphylococcus aureus and Listeria innocua were the most resistant bacteria towards GABA-EFS. In addition, GABA production was confirmed by pre-staining thin layer chromatography and fourier transform infrared spectroscopy. The results suggested that the GABA-EFS could be applied in the food industry as a functional product.
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References
L. Day, R.B. Seymour, K.F. Pitts, I. Konczak, L. Lundin, Incorporation of functional ingredients into foods. Trends Food Sci. Technol. 20(9), 388–395 (2009)
S.H. Al-Sheraji, A. Ismail, M.Y. Manap, S. Mustafa, R.M. Yusof, F.A. Hassan, Prebiotics as functional foods: a review. J. Funct. Foods 5(4), 1542–1553 (2013)
J.M. Villegas, L. Brown, G.S. de Giori, E.M. Hebert, Optimization of batch culture conditions for GABA production by Lactobacillus brevis CRL 1942, isolated from quinoa sourdough. LWT-Food Sci. Technol. 67, 22–26 (2016)
K. Mahmood, H. Kamilah, A.K. Alias, F. Ariffin, Nutritional and therapeutic potentials of rambutan fruit (Nephelium lappaceum L.) and the by-products: a review. J. Food Meas. Charact. 12, 1556–1571 (2018)
K.B. Park, S.H. Oh, Production of yogurt with enhanced levels of gamma-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Bioresour. Technol. 98(8), 1675–1679 (2007)
R. Dhakal, V.K. Bajpai, K.H. Baek, Production of GABA (γ-aminobutyric acid) by microorganisms: a review. Braz. J. Microbiol. 43(4), 1230–1241 (2012)
H. Li, Y. Cao, Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39(5), 1107–1116 (2010)
H. Li, T. Qiu, D. Gao, Y. Cao, Medium optimization for production of gamma-aminobutyric acid by Lactobacillus brevis NCL912. Amino Acids 38(5), 1439–1445 (2010)
H. Jooyandeh, Soy products as healthy and functional foods. Middle East J. Sci. Res. 7(1), 71–80 (2011)
R. Karimi, M.H. Azizi, M. Ghasemlou, M. Vaziri, Application of inulin in cheese as prebiotic, fat replacer and texturizer: a review. Carbohydr. Polym. 119, 85–100 (2015)
M.A. Mensink, H.W. Frijlink, K. van der Voort Maarschalk, W.L. Hinrichs, Inulin, a flexible oligosaccharide I: review of its physicochemical characteristics. Carbohydr. Polym. 130, 405–419 (2015)
J.M. Berg, J.L. Tymoczko, L. Stryer, Biochemistry, 5th edn. (W H freeman, New York, 2002)
H. Li, T. Qiu, Y. Cao, J. Yang, Z. Huang, Pre-staining paper chromatography method for quantification of γ-aminobutyric acid. J. Chromatogr. A 1216(25), 5057–5060 (2009)
N.T. Hoyle, J.H. Merritt, Quality of fish protein hydrolysates from herring (Clupea harengus). J. Food Sci. 59(1), 76–79 (1994)
J. Adler-Nissen, Enzymic Hydrolysis of Food Proteins, 1st edn. (Elsevier Applied Science, London, 1986), pp. 110–169
B.A. Behbahani, F. Shahidi, F.T. Yazdi, S.A. Mortazavi, M. Mohebbi, Antioxidant activity and antimicrobial effect of tarragon (Artemisia dracunculus) extract and chemical composition of its essential oil. J. Food Meas. Charact. 11(2), 847–863 (2017)
B.A. Behbahani, F. Shahidi, F.T. Yazdi, S.A. Mortazavi, M. Mohebbi, Use of Plantago major seed mucilage as a novel edible coating incorporated with Anethum graveolens essential oil on shelf life extension of beef in refrigerated storage. Int. J. Biol. Macromol. 94, 515–526 (2017)
M. Noshad, M. Hojjati, B.A. Behbahani, Black Zira essential oil: chemical compositions and antimicrobial activity against the growth of some pathogenic strain causing infection. Microb. Pathog. 116, 153–157 (2018)
X. Li, X. Shi, Y. Jin, F. Ding, Y. Du, Controllable antioxidative xylan–chitosan Maillard reaction products used for lipid food storage. Carbohydr. Polym. 91(1), 428–433 (2013)
J. Xie, M. Du, M. Shen, T. Wu, L. Lin, Physico-chemical properties, antioxidant activities and angiotensin-I converting enzyme inhibitory of protein hydrolysates from Mung bean (Vigna radiate). Food Chem. 270, 243–250 (2019)
Q. Deng, L. Wang, F. Wei, B. Xie, F. Huang, W. Huang, J. Shin, Q. Huang, B. Tian, S. Xue, Functional properties of protein isolates, globulin and albumin extracted from Ginkgo biloba seeds. Food Chem. 124(4), 1458–1465 (2011)
D. Betancur-Ancona, G. Peraza-Mercado, Y. Moguel-Ordonez, S. Fuertes-Blanco, Physicochemical characterization of lima bean (Phaseolus lunatus) and Jack bean (Canavalia ensiformis) fibrous residues. Food Chem. 84(2), 287–295 (2004)
T.J. Kim, C.H. Sung, Y.J. Kim, B.M. Jung, E.R. Kim, W.S. Choi, H.K. Jung, H.N. Chun, W.J. Kim, S.H. Yoo, Effects of a soaking-fermentation-drying process on the isoflavone and γ-aminobutyric acid contents of soybean. Food Sci. Biotechnol. 16(1), 83–89 (2007)
H. Aoki, I. Uda, K. Tagami, Y. Furuya, Y. Endo, K. Fujimoto, The production of a new tempeh-like fermented soybean containing a high level of γ-aminobutyric acid by anaerobic incubation with Rhizopus. Biosci. Biotechnol. Biochem. 67(5), 1018–1023 (2003)
J.Y. Kim, M.Y. Lee, G.E. Ji, Y.S. Lee, K.T. Hwang, Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int. J. Food Microbiol. 130(1), 12–16 (2009)
E. Barrett, R.P. Ross, P.W. O’toole, G.F. Fitzgerald, C. Stanton, γ-Aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 113(2), 411–417 (2012)
N. Komatsuzaki, J. Shima, S. Kawamoto, H. Momose, T. Kimura, Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22(6), 497–504 (2005)
I. Amadou, G.W. Le, Y.H. Shi, S. Jin, Reducing, radical scavenging, and chelation properties of fermented soy protein meal hydrolysate by Lactobacillus plantarum Lp6. Int. J. Food Prop. 14(3), 654–665 (2011)
T.Ž. Krunić, N.S. Obradović, M.B. Rakin, Application of whey protein and whey protein hydrolysate as protein based carrier for probiotic starter culture. Food Chem. (2019). https://doi.org/10.1016/j.foodchem.2019.04.062
B. Alizadeh Behbahani, A.A. Imani Fooladi, Development of a novel edible coating made by Balangu seed mucilage and Feverfew essential oil and investigation of its effect on the shelf life of beef slices during refrigerated storage through intelligent modeling. J. Food Saf. 38, e12443 (2018)
A.A. Rushdy, E.Z. Gomaa, Antimicrobial compounds produced by probiotic Lactobacillus brevis isolated from dairy products. Ann. Microbiol. 63(1), 81–90 (2013)
S. Sanjukta, A.K. Rai, Production of bioactive peptides during soybean fermentation and their potential health benefits. Trends Food Sci. Technol. 50, 1–10 (2016)
F.C.S. Vasconcellos, A.L. Woiciechowski, V.T. Soccol, D. Mantovani, C.R. Soccol, Antimicrobial and antioxidant properties of-conglycinin and glycinin from soy protein isolate. Int. J. Curr. Microbiol. Appl. Sci. 3(8), 144–157 (2014)
M. Zasloff, Antimicrobial peptides of multicellular organisms. Nature 415(6870), 389–395 (2002)
K. Matsuzaki, Control of cell selectivity of antimicrobial peptides. Biochim. Biophys. Acta 1788(8), 1687–1692 (2009)
C.F. De Oliveira, A.P.F. Corrêa, D. Coletto, D.J. Daroit, F. Cladera-Olivera, A. Brandelli, Soy protein hydrolysis with microbial protease to improve antioxidant and functional properties. J. Food Sci. Technol. 52(5), 2668–2678 (2015)
R. Farng, S. Mrha, U.S. Patent No. 7,928,147 (U.S. Patent and Trademark Office, Washington, DC, 2011)
X. Wang, G.R. Gibson, Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J. Appl. Bacteriol. 75(4), 373–380 (1993)
M. Mohammadian, A. Madadlou, Characterization of fibrillated antioxidant whey protein hydrolysate and comparison with fibrillated protein solution. Food Hydrocoll. 52, 221–230 (2016)
L. Khadidja, C. Asma, B. Mahmoud, E. Meriem, Alginate/gelatin crosslinked system through Maillard reaction: preparation, characterization and biological properties. Polym. Bull. 74(12), 4899–4919 (2017)
B. Kong, Y.L. Xiong, Antioxidant activity of zein hydrolysates in a liposome system and the possible mode of action. J. Agric. Food Chem. 54(16), 6059–6068 (2006)
Y. Li, B. Jiang, T. Zhang, W. Mu, J. Liu, Antioxidant and free radical-scavenging activities of chickpea protein hydrolysate (CPH). Food Chem. 106(2), 444–450 (2008)
X. Peng, B. Kong, X. Xia, Q. Liu, Reducing and radical-scavenging activities of whey protein hydrolysates prepared with Alcalase. Int. Dairy J. 20(5), 360–365 (2010)
H.C. Wu, H.M. Chen, C.Y. Shiau, Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Res. Int. 36(9–10), 949–957 (2003)
N. Cumby, Y. Zhong, M. Naczk, F. Shahidi, Antioxidant activity and water-holding capacity of canola protein hydrolysates. Food Chem. 109(1), 144–148 (2008)
C.Y. Chang, K.C. Wu, S.H. Chiang, Antioxidant properties and protein compositions of porcine haemoglobin hydrolysates. Food Chem. 100(4), 1537–1543 (2007)
K. Saito, D.H. Jin, T. Ogawa, K. Muramoto, E. Hatakeyama, T. Yasuhara, K. Nokihara, Antioxidative properties of tripeptide libraries prepared by the combinatorial chemistry. J. Agric. Food Chem. 51(12), 3668–3674 (2003)
J.H. Yang, J.L. Mau, P.T. Ko, L.C. Huang, Antioxidant properties of fermented soybean broth. Food Chem. 71(2), 249–254 (2000)
K.N. Pearce, J.E. Kinsella, Emulsifying properties of proteins: evaluation of a turbidimetric technique. J. Agric. Food Chem. 26(3), 716–723 (1978)
S. Jung, P.A. Murphy, L.A. Johnson, Physicochemical and functional properties of soy protein substrates modified by low levels of protease hydrolysis. J. Food Sci. 70(2), C180–C187 (2005)
G.A. Gbogouri, M. Linder, J. Fanni, M. Parmentier, Influence of hydrolysis degree on the functional properties of salmon byproducts hydrolysates. J. Food Sci. 69(8), C615–C622 (2004)
S. Barbut, Determining Water and Fat Holding. Methods of Testing Protein Functionality (Springer, Berlin, 1999), pp. 186–225
A. Achouri, W. Zhang, X. Shiying, Enzymatic hydrolysis of soy protein isolate and effect of succinylation on the functional properties of resulting protein hydrolysates. Food Res. Int. 31(9), 617–623 (1998)
M.A. Mune Mune, Influence of degree of hydrolysis on the functional properties of cowpea protein hydrolysates. J. Food Process. Preserv. 39(6), 2386–2392 (2015)
J. Yu, G. Wang, X. Wang, Y. Xu, S. Chen, X. Wang, L. Jiang, Improving the freeze-thaw stability of soy protein emulsions via combing limited hydrolysis and Maillard-induced glycation. LWT-Food Sci. Technol. 91, 63–69 (2018)
M.C. Gómez-Guillén, M.E. López Caballero, A. Alemán, A.L. de Lacey, B. Giménez, P. Montero García, Antioxidant and antimicrobial peptide fractions from squid and tuna skin gelatin, in Sea By-Products as Real Material: New Ways of Application, ed. by E. Le Bihan (Transworld Research Network Signpost, Kerala, 2010), pp. 89–115
A. Barth, Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767(9), 1073–1101 (2007)
J. Yu, G. Wang, X. Wang, Y. Xu, S. Chen, X. Wang, L. Jiang, Improving the freeze-thaw stability of soy protein emulsions via combing limited hydrolysis and Maillard-induced glycation. LWT 91, 63–69 (2018)
K. Elavarasan, B.A. Shamasundar, F. Badii, N. Howell, Angiotensin I-converting enzyme (ACE) inhibitory activity and structural properties of oven-and freeze-dried protein hydrolysate from fresh water fish (Cirrhinus mrigala). Food Chem. 206, 210–216 (2016)
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The authors of this paper acknowledge the support of Ferdowsi University of Mashhad (FUM) through Project 46386.
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Zareie, Z., Tabatabaei Yazdi, F. & Mortazavi, S.A. Optimization of gamma-aminobutyric acid production in a model system containing soy protein and inulin by Lactobacillus brevis fermentation. Food Measure 13, 2626–2636 (2019). https://doi.org/10.1007/s11694-019-00183-8
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DOI: https://doi.org/10.1007/s11694-019-00183-8