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Evaluation of a Malaysian soy sauce koji strain Aspergillus oryzae NSK for γ-aminobutyric acid (GABA) production using different native sugars

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Abstract

In this study, a selected γ-aminobutyric acid (GABA)-rich Malaysian strain Aspergillus oryzae NSK was collected from soy sauce koji. The strain was used to explore the effect of using renewable native sugar syrup, sugarcane, nipa, and molasses as fermentable substrates for developing a novel functional GABA soy sauce. We evaluated the strain using the chosen native sugars for 7 days using shake flask fermentation at 30 °C. The results showed optimum GABA concentration was achieved using cane molasses as the fermentable substrate (354.08 mg/L), followed by sugarcane syrup (320.7 mg/L) and nipa syrup (232.07 mg/L). Cane molasses was subsequently utilized as a substrate to determine the most suitable concentration for A. oryzae NSK to enhance GABA production and was determined as 50% g/L of glucose standard cane molasses. Our findings indicate that cane molasses can be used as a GABA-rich ingredient to develop a new starter culture for A. oryzae NSK soy sauce production.

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Abbreviations

P :

GABA concentration (mg/L)

S :

Substrate concentration (g/L)

S 0 :

Initial substrate concentration (g/L)

t :

Fermentation time (h−1)

X :

Cell concentration (g/L)

X m :

Maximum cell concentration (g/L)

X 0 :

Initial cell concentration (g/L)

Y p/s :

Yield factor for product on cell (mg/g)

Y x/s :

Yield factor for cell on substrate (g/g)

K s :

Monod growth saturation coefficient (g/L)

μ m :

Maximum specific growth rate (h)

References

  1. Zonghua XQTWA. Analysis of the source of antioxidant compounds in Zhenjiang vinegar. Food Ferment Indust 3: 11 (2005)

  2. Roohinejad S, Omidizadeh A, Mirhosseini H, Rasti B, Saari N, Mustafa S, Yusof RM, Hussin ASM, Hamid A, Manap MYA. Effect of hypocholesterolemic properties of brown rice varieties containing different gamma aminobutyric acid (GABA) levels on Sprague-Dawley male rats. J Food Agric Environ 7: 197–203 (2009)

    CAS  Google Scholar 

  3. Roohinejad S, Omidizadeh A, Mirhosseini H, Saari N, Mustafa S, Yusof RM, Hussin AS, Hamid A, Abd Manap MY. Effect of pre-germination time of brown rice on serum cholesterol levels of hypercholesterolaemic rats. J Sci Food Agric 90: 245–51 (2010)

    Article  CAS  Google Scholar 

  4. Okada T, Sugishita T, Murakami T, Murai H, Saikusa T, Horino T, Onoda A, Kajimoto O, Takahashi R, Takahashi T. Effect of the defatted rice germ enriched with GABA for sleeplessness, depression, autonomic disorder by oral administration. J-Jap Soc Food Sci Technol 47: 596–603 (2000)

    Article  CAS  Google Scholar 

  5. Han D, Kim HY, Lee HJ, Shim I, Hahm DH. Wound healing activity of gamma-aminobutyric acid (GABA) in rats. J Microbiol Biotechnol 17: 1661–9 (2007)

    CAS  Google Scholar 

  6. Choi W-c, Reid SNS, Ryu J-k, Kim Y, Jo Y-H, Jeon BH. Effects of γ-aminobutyric acid-enriched fermented sea tangle (Laminaria japonica) on brain derived neurotrophic factor-related muscle growth and lipolysis in middle aged women. Algae 31: 175–187 (2016)

    Article  Google Scholar 

  7. Ab Kadir S, Wan-Mohtar WA, Mohammad R, Abdul Halim Lim S, Sabo Mohammed A, Saari N. Evaluation of commercial soy sauce koji strains of Aspergillus oryzae for gamma-aminobutyric acid (GABA) production. J Ind Microbiol Biotechnol 43: 1387–95 (2016)

    Article  CAS  Google Scholar 

  8. Jorge JM, Nguyen AQ, Perez-Garcia F, Kind S, Wendisch VF. Improved fermentative production of gamma-aminobutyric acid via the putrescine route: Systems metabolic engineering for production from glucose, amino sugars, and xylose. Biotechnol Bioeng 114: 862–873 (2016)

    Article  Google Scholar 

  9. Cho YR, Chang JY, Chang HC. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol 17: 104–9 (2007)

    CAS  Google Scholar 

  10. Park K-B, Oh S-H. Production of yogurt with enhanced levels of gamma-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Biores Technol 98: 1675–1679 (2007)

    Article  CAS  Google Scholar 

  11. Chiu CH, Ni KH, Guu YK, Pan TM. Production of red mold rice using a modified Nagata type koji maker. Appl Microbiol Biot 73: 297–304 (2006)

    Article  CAS  Google Scholar 

  12. Nomura M, Kimoto H, Someya Y, Furukawa S, Suzuki I. Production of gamma-aminobutyric acid by cheese starters during cheese ripening. J Dairy Sci 81: 1486–91 (1998)

    Article  CAS  Google Scholar 

  13. Kim JY, Lee MY, Ji GE, Lee YS, Hwang KT. Production of gamma-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int J Food Microbiol 130: 12–6 (2009)

    Article  CAS  Google Scholar 

  14. Saikusa T, Horino T, Mori Y. Accumulation of γ-aminobutyric acid (GABA) in the rice germ during water soaking. Biosci Biotechnol Biochem 58: 2291–2292 (1994)

    Article  CAS  Google Scholar 

  15. Coda R, Rizzello CG, Gobbetti M. Use of sourdough fermentation and pseudo-cereals and leguminous flours for the making of a functional bread enriched of gamma-aminobutyric acid (GABA). Int J Food Microbiol 137: 236–45 (2010)

    Article  CAS  Google Scholar 

  16. Aoki H, Furuya Y, Endo Y, Fujimoto K. Effect of gamma-aminobutyric acid-enriched tempeh-like fermented soybean (GABA-Tempeh) on the blood pressure of spontaneously hypertensive rats. Biosci Biotechnol Biochem 67: 1806–8 (2003)

    Article  CAS  Google Scholar 

  17. Wisuthiphaet N, Napathorn SC. Optimisation of the use of products from the cane sugar industry for poly(3-hydroxybutyrate) production by Azohydromonas lata DSM 1123 in fed-batch cultivation. Process Biochem 51: 352–361 (2016)

    Article  CAS  Google Scholar 

  18. Skountzou P, Soupioni M, Bekatorou A, Kanellaki M, Koutinas A, Marchant R, Banat I. Lead (II) uptake during baker’s yeast production by aerobic fermentation of molasses. Proc Biochem 38: 1479–1482 (2003)

    Article  CAS  Google Scholar 

  19. Olbrich H. The molasses. Principles Sugar Technol 3: 511–697 (1963)

    Google Scholar 

  20. Calabia BP, Tokiwa Y. Production of D-lactic acid from sugarcane molasses, sugarcane juice and sugar beet juice by Lactobacillus delbrueckii. Biotechnol Lett 29: 1329–32 (2007)

    Article  CAS  Google Scholar 

  21. Law SV, Abu Bakar F, Mat Hashim D, Abdul Hamid A. Popular fermented foods and beverages in Southeast Asia. Intern Food Res J 18: 475–484 (2011)

    Google Scholar 

  22. Sharma M, Patel SN, Lata K, Singh U, Krishania M, Sangwan RS, Singh SP. A novel approach of integrated bioprocessing of cane molasses for production of prebiotic and functional bioproducts. Bioresour Technol 219: 311–318 (2016)

    Article  CAS  Google Scholar 

  23. Miloski K, Wallace K, Fenger A, Schneider E, Bendinskas K. Comparison of biochemical and chemical digestion and detection methods for carbohydrates. American J Undergraduate Res 7: 48–52 (2008)

    Google Scholar 

  24. Rossi A, Villarreal M, Juárez M, Sammán N, “Anales de la Asociación Química Argentina,” ed. SciELO Argentina, pp. 99–108 (2004).

  25. Dunko A, Dovletoglou A. Moisture assay of an antifungal by near-infrared diffuse reflectance spectroscopy. J Pharm Biomed Anal 28: 145–54 (2002)

    Article  CAS  Google Scholar 

  26. Wan-Mohtar WA, Ab Kadir S, Saari N. The morphology of Ganoderma lucidum mycelium in a repeated-batch fermentation for exopolysaccharide production. Biotechnol Rep (Amst) 11: 2–11 (2016)

    Article  Google Scholar 

  27. Tamunaidu P, Matsui N, Okimori Y, Saka S. Nipa (Nypa fruticans) sap as a potential feedstock for ethanol production. Biomass Bioen 52: 96–102 (2013)

    Article  CAS  Google Scholar 

  28. Nakata H, Tamura M, Shintani T, Gomi K. Evaluation of baker’s yeast strains exhibiting significant growth on Japanese beet molasses and compound analysis of the molasses types. J Biosci Bioeng 117: 715–9 (2014)

    Article  CAS  Google Scholar 

  29. Iskandar HM, Casu RE, Fletcher AT, Schmidt S, Xu J, Maclean DJ, Manners JM, Bonnett GD. Identification of drought-response genes and a study of their expression during sucrose accumulation and water deficit in sugarcane culms. BMC Plant Biol 11: 12 (2011)

    Article  CAS  Google Scholar 

  30. Naik G. Biochemical and molecular analysis of sugarcane glutamate decarboxylase. Intern J Bioas 2: 1011–1016 (2013)

    Google Scholar 

  31. Shibuya I, Tsuchiya K, Tamura G, Ishikawa T, Hara S. Overproduction of an α-amylase/glucoamylase fusion protein in Aspergillus oryzae using a high expression vector. Biosci Biotechnol Biochem 56: 1674–1675 (1992)

    Article  CAS  Google Scholar 

  32. Kumar S, Punekar NS, SatyaNarayan V, Venkatesh K. Metabolic fate of glutamate and evaluation of flux through the 4‐aminobutyrate (GABA) shunt in Aspergillus niger. Biotechnol Bioeng 67: 575–584 (2000)

    Article  CAS  Google Scholar 

  33. Su YC, Wang JJ, Lin TT, Pan TM. Production of the secondary metabolites gamma-aminobutyric acid and monacolin K by Monascus. J Ind Microbiol Biotechnol 30: 41–6 (2003)

    Article  CAS  Google Scholar 

  34. Hirose N, Ujihara K, Teruya R, Maeda G, (2008).

  35. Deacon JW. Fungal biology. John Wiley & Sons (2013)

  36. Shelp BJ, Bown AW, McLean MD. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4: 446–452 (1999)

    Article  CAS  Google Scholar 

  37. Park SC, Baratti J. Batch fermentation kinetics of sugar beet molasses by Zymomonas mobilis. Biotechnol Bioeng 38: 304–13 (1991)

    Article  CAS  Google Scholar 

  38. Sun B, Zhou L, Jia X, Sung C. Response surface modeling for y-aminobutyric acid production by Monascus pilosus GM100 under solid-state fermentation. African J Biotechnol 7 (2008)

  39. Ratanaburee A, Kantachote D, Charernjiratrakul W, Penjamras P, Chaiyasut C. Enhancement of γ-aminobutyric acid in a fermented red seaweed beverage by starter culture Lactobacillus plantarum DW12. Elect J Biotechnol 14: 1–1 (2011)

    Google Scholar 

  40. Wang J-J, Lee C-L, Pan T-M. Improvement of monacolin K, γ-aminobutyric acid and citrinin production ratio as a function of environmental conditions of Monascus purpureus NTU 601. J Ind Microbiol Biotechnol 30: 669–676 (2003)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to extend our gratitude to the Ministry of Higher Education (MOHE) Malaysia for the financial support awarded to Prof Dr Nazamid Saari under the FRGS (Vot No: 5523380).

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Hajar-Azhari, S., Wan-Mohtar, W.A.A.Q.I., Ab Kadir, S. et al. Evaluation of a Malaysian soy sauce koji strain Aspergillus oryzae NSK for γ-aminobutyric acid (GABA) production using different native sugars. Food Sci Biotechnol 27, 479–488 (2018). https://doi.org/10.1007/s10068-017-0289-6

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  • DOI: https://doi.org/10.1007/s10068-017-0289-6

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