Sains Malaysiana 54(2)(2025): 483-492

http://doi.org/10.17576/jsm-2025-5402-14

Production and Acceptance of Gamma-Aminobutyric Acid (GABA)-Kimchi using Tetragenococcus halophilus and Monosodium Glutamate

(Penghasilan dan Penerimaan Kimchi yang Mengandungi Asid Gamma-Aminobutirik (GABA) menggunakan Tetragenococcus halophilus dan Monosodium Glutamat)

FATEEN AQLIMA HANIEM AB JABAR¹, CHONG SHIN YEE¹, ZUL ILHAM², NURUL AQILAH MOHD ZAINI³, MUHAMAD HAFIZ ABD RAHIM⁴, NUR ASYIQIN ZAHIA-AZIZAN¹ & WAN ABD AL QADR IMAD WAN-MOHTAR^1,*

¹Functional Omics and Bioprocess Development Laboratory, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
²Environmental Science and Management Program, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
³Department of Food Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia
⁴Faculty of Food and Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia

Diserahkan: 23 Ogos 2024/Diterima: 12 November 2024

Abstract

The addition of gamma-aminobutyric acid (GABA) to fermented foods has been progressively expanded to produce ‘Superfood’. In this study, Tetragenococcus halophilus was extracted from soy sauce moromi from local factory and evaluated for its potential of Gamma-Aminobutyric Acid (GABA) production in kimchi fermentation. There were four different formulations that were fermented for 20 days. Kimchi fermentation was performed on kimchi added with Monosodium Glutamate (MSG) (T1), kimchi inoculated with T. halophilus (T2), kimchi with combined MSG and T. halophilus (T3), and plain kimchi with no additional starter as a control (C), respectively. A spectral HPLC analysis confirmed that the control sample (C) obtained the highest GABA with 10.90 mg/L followed by T2 with 6.02 mg/L, T1 with 5.72 mg/L, and the lowest content of GABA is produced by T3 with 3.74 mg/L. Sensory analysis was performed by a total of 50 panellists examined the colour, flavour, texture, taste, and overall acceptance of kimchi samples. Kimchi with MSG (T1) received the highest scores for overall acceptance including flavour and taste. This study demonstrated the development of GABA-kimchi using T. halophilus and MSG as future food comprising substantial nutritional profile and improved sensory characteristics.

Keywords: Fermentation; GABA; kimchi; MSG; superfood; Tetragenococcus halophilus

Abstrak

Penambahan asid gamma-aminobutirik (GABA) kepada makanan yang ditapai telah diperluaskan secara berperingkat untuk menghasilkan makanan super. Dalam kajian ini, Tetragenococcus halophilustelah diekstrak daripada moromi kicap daripada kilang tempatan dan dinilai untuk potensi penghasilan asid gamma-aminobutirik (GABA) dalam penapaian kimchi. Terdapat empat formulasi berbeza yang ditapai selama 20 hari. Penapaian kimchi dilakukan pada kimchi yang ditambah dengan Monosodium Glutamat (MSG) (T1), kimchi yang digabungkan dengan T. halophilus (T2), kimchi dengan gabungan MSG dan T. halophilus (T3) dan kimchi biasa tanpa pemula tambahan sebagai kawalan (C), secara berturutan. Analisis HPLC spektrum mengesahkan bahawa sampel kawalan (C) memperoleh GABA tertinggi dengan 10.90 mg/L diikuti oleh T2 dengan 6.02 mg/L, T1 dengan 5.72 mg/L dan kandungan terendah GABA dihasilkan oleh T3 dengan 3.74 mg/L. Analisis deria telah dilakukan terhadap sejumlah 50 ahli panel yang meneliti warna, rasa, tekstur, rasa dan penerimaan keseluruhan sampel kimchi. Kimchi dengan MSG (T1) menerima markah tertinggi untuk penerimaan keseluruhan termasuk perasa dan rasa. Kajian ini menunjukkan bahawa pengeluaran GABA-kimchi menggunakan T. halophilus dan MSG sebagai makanan masa depan dengan profil nutrisi pemakanan yang tinggi dan ciri deria yang lebih baik.

Kata kunci: Fermentasi; GABA; kimchi; makanan super; MSG; Tetragenococcus halophilus

RUJUKAN

Azizan, N., Lim, T., Raseetha, S. & Wan Mohtar, W.A.A.-Q.I. 2022. Development of γ-aminobutyric acid (GABA)-rich yoghurt using Tetragenococcus halophilus strain KBC isolated from a commercial soy sauce moromi. Food Research 6(6): 39-47.

Chung, H-K., Yang, H.J., Shin, D. & Chung, K.R. 2016. Aesthetics of Korean foods: The symbol of Korean culture. Journal of Ethnic Foods 3(3): 178-188.

Cui, Y., Miao, K., Niyaphorn, S. & Qu, X. 2020. Production of gamma-aminobutyric acid from lactic acid bacteria: A systematic review. International Journal of Molecular Sciences 21(3): 995.

Devanthi, P.V.P., Linforth, R., Onyeaka, H. & Gkatzionis, K. 2018. Effects of co-inoculation and sequential inoculation of Tetragenococcus halophilus and Zygosaccharomyces rouxii on soy sauce fermentation. Food Chemistry 240: 1-8.

Di Cagno, R., Mazzacane, F., Rizzello, C.G., De Angelis, M., Giuliani, G., Meloni, M., De Servi, B. & Gobbetti, M. 2010. Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: Functional grape must beverage and dermatological applications. Applied Microbiology and Biotechnology 86: 731-741.

Faizal, F., Ahmad, N., Yaacob, J., Halim-Lim, S.A. & Rahim, M.A. 2023. Food processing to reduce antinutrients in plant-based foods. International Food Research Journal 30(1): 25-45.

Hajar-Azhari, S., Ab Jabar, F.A.H., Ilham, Z., Abd Rahim, M.H., Zaini, N.A.M. & Wan, W.A.A.Q.I. 2024. Flavor compound profiles and enhancement strategies in the kimchi-making process. Food Bioscience 2024: 105385.

Hepsomali, P., Groeger, J.A., Nishihira, J. & Scholey, A. 2020. Effects of oral gamma-aminobutyric acid (GABA) administration on stress and sleep in humans: A systematic review. Frontiers in Neuroscience 14: 559962.

Hussin, F.S., Chay, S.Y., Hussin, A.S.M., Wan Ibadullah, W.Z., Muhialdin, B.J., Abd Ghani, M.S. & Saari, N. 2021. GABA enhancement by simple carbohydrates in yoghurt fermented using novel, self-cloned Lactobacillus plantarum Taj-Apis362 and metabolomics profiling. Scientific Reports 11(1): 9417. https://pmc.ncbi.nlm.nih.gov/articles/PMC8093275/pdf/41598_2021_Article_88436.pdf

Jang, D-J., Chung, K.R., Yang, H.J., Kim, K-S. & Kwon, D.Y. 2015. Discussion on the origin of kimchi, representative of Korean unique fermented vegetables. Journal of Ethnic Foods 2(3): 126-136.

Jung, J.Y., Lee, S.H. & Jeon, C.O. 2014. Kimchi microflora: History, current status, and perspectives for industrial kimchi production. Applied Microbiology and Biotechnology 98: 2385-2393.

Kazmi, Z., Fatima, I., Perveen, S. & Malik, S.S. 2017. Monosodium glutamate: Review on clinical reports. International Journal of Food Properties 20(Sup2): 1807-1815.

Kwon, S-Y., Garcia, C.V., Song, Y-C. & Lee, S-P. 2016. GABA-enriched water dropwort produced by co-fermentation with Leuconostoc mesenteroides SM and Lactobacillus plantarum K154. Lwt 73: 233-238.

Lee, K.W., Shim, J.M., Yao, Z., Kim, J.A. & Kim, J.H. 2018. Properties of kimchi fermented with GABA-producing lactic acid bacteria as a starter. Journal of Microbiology and Biotechnology 28(4): 534-541.

Lee, M-E., Jang, J-Y., Lee, J-H., Park, H-W., Choi, H-J. & Kim, T-W. 2015. Starter cultures for kimchi fermentation. Journal of Microbiology and Biotechnology 25(5): 559-568.

Lim, K., & Koh, J. 2021. Fermented foods and probiotic beverages in Korea. In Probiotic Beverages pp. 61-80. Academic Press.

Löliger, J. 2000. Function and importance of glutamate for savory food. The Journal of Nutrition 130(4): 915S-920S.

Lyu, C., Zhao, W., Peng, C., Hu, S., Fang, H., Hua, Y., Yao, S., Huang, J. & Mei, L. 2018. Exploring the contributions of two glutamate decarboxylase isozymes in Lactobacillus brevis to acid resistance and γ-aminobutyric acid production. Microbial Cell Factories 17: 180.

Phuengjayaem, S., Kuncharoen, N., Booncharoen, A., Ongpipattanakul, B. & Tanasupawat, S. 2021. Genome analysis and optimization of γ-aminobutyric acid (GABA) production by lactic acid bacteria from plant materials. The Journal of General and Applied Microbiology 67(4): 150-161.

Rakotosamimanana, V.R. & De Kock, H.L. 2020. Sensory studies with low-income, food-insecure consumers. Current Opinion in Food Science 33: 108-114.

Rayavarapu, B., Tallapragada, P. & Usha, M. 2019. Statistical optimization of γ-aminobutyric acid production by response surface methodology and artificial neural network models using Lactobacillus fermentum isolated from palm wine. Biocatalysis and Agricultural Biotechnology 22: 101362.

Sassi, S., Ilham, Z., Jamaludin, N.S., Halim-Lim, S.A., Shin Yee, C., Weng Loen, A.W., Poh Suan, O., Ibrahim, M.F. & Wan-Mohtar, W.A.A.Q.I. 2022. Critical optimized conditions for gamma-aminobutyric acid (GABA)-producing Tetragenococcus halophilus strain KBC from a commercial soy sauce Moromi in batch fermentation. Fermentation 8(8): 409.

Seok, J-H., Park, K-B., Kim, Y-H., Bae, M-O., Lee, M-K. & Oh, S-H. 2008. Production and characterization of kimchi with enhanced levels of γ-aminobutyric acid. Food Science and Biotechnology 17(5): 940-946.

Surya, R. & Lee, A.G.Y. 2022. Exploring the philosophical values of kimchi and kimjang culture. Journal of Ethnic Foods 9(1): 20.

Susilowati, S., Laia, S. & Purnomo, H. 2018. The effect of salt concentration and fermentation time on pH value, total acidity and microbial characteristic of pickled ginger (Zingiber officinale Rosc.). International Food Research Journal 25(6): 2301-2306.

Ting Wong, C.G., Bottiglieri, T. & Carter Snead III, O. 2003. GABA, γ‐hydroxybutyric acid, and neurological disease. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society 54(S6): S3-S12.

Udomsil, N., Rodtong, S., Choi, Y.J., Hua, Y. & Yongsawatdigul, J. 2011. Use of Tetragenococcus halophilus as a starter culture for flavor improvement in fish sauce fermentation. Journal of Agricultural and Food Chemistry 59(15): 8401-8408.

Wan-Mohtar, W.A.A.Q.I., Ilham, Z., Jamaludin, A.A., David, W. & Mohd Zaini, N.A. 2022. Fermented foods as alternative functional foods during post-pandemic in Asia. Frontiers in Food Science and Technology 2: 1047970.

Wan-Mohtar, W.A.A.Q.I., Sohedein, M.N.A., Ibrahim, M.F., Ab Kadir, S., Suan, O.P., Weng Loen, A.W., Sassi, S. & Ilham, Z. 2020. Isolation, identification, and optimization of γ-aminobutyric acid (GABA)-producing Bacillus cereus strain KBC from a commercial soy sauce moromi in submerged-liquid fermentation. Processes 8(6): 652.

Yang, S.Y., Lu, Z.X., Lu, F.X., Bie, X.M., Sun, L.J. & Zeng, X.X. 2006. A simple method for rapid screening of bacteria with glutamate decarboxylase activities. Journal of Rapid Methods & Automation in Microbiology 14(3): 291-298.

Yee, C.S., Sohedein, M.N.A., Suan, O.P., Loen, A.W.W., Abd Rahim, M.H., Soumaya, S., Ilham, Z. & Wan, W.A.A.Q.I. 2021. The production of functional γ-aminobutyric acid Malaysian soy sauce koji and moromi using the trio of Aspergillus oryzae NSK, Bacillus cereus KBC, and the newly identified Tetragenococcus halophilus KBC in liquid-state fermentation. Future Foods 4: 100055.

Yilmaz-Ersan, L. & Kurdal, E. 2014. The production of set-type-bio-yoghurt with commercial probiotic culture. International Journal of Chemical Engineering and Applications 5(5): 402.

*Pengarang untuk surat-menyurat; email: qadyr@um.edu.my