Skip to main content
Log in

Evaluation of gamma-aminobutyric acid (GABA) production by Lactobacillus plantarum using two-step fermentation

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Lactic acid bacteria (Lactobacillus plantarum KCTC 3103) were fermented to produce gamma-aminobutyric acid (GABA). The conditions of the modified synthetic medium were optimized as 5 g/L glucose, 10 g/L yeast extract, 100 g/L rice bran extract, and 1.0 g/L ascorbic acid for GABA production. Single-step fermentation of cell growth and GABA production with a modified synthetic medium was higher than those with an MRS medium. Two-step fermentation was evaluated by separating the cell growth and GABA production under a modified synthetic medium. The cell concentration of 1.65 g dcw/L produced by the modified synthetic medium was higher than that of 1.0 g dcw/L produced by the MRS medium at 36 h from the first step of two-step fermentation. The highest GABA production of L. plantarum KCTC 3103 was 0.67 g/L with monosodium glutamate addition at 60 h in the second step of fermentation. Two-step fermentation with the modified synthetic medium is suitable for GABA production because of its high GABA productivity and favorable cell growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ueno H (2000) Enzymatic and structural aspects on glutamate decarboxylase. J Mol Catal B Enzyme 10:67–79

    Article  CAS  Google Scholar 

  2. Jannoey P, Niamsup H, Lumyong S, Tajima S, Nomura M, Chairote G (2010) γ-aminobutyric acid (GABA) accumulations in rice during germination. Chiang Mai J Sci 66:2600–2605

    Google Scholar 

  3. Wang HF, Tsai YS, Lin ML, Ou ASM (2006) Comparison of bioactive compounds in GABA tea and green tea produced in Taiwan. Food Chem 96:648–653

    Article  CAS  Google Scholar 

  4. Youn YS, Park JK, Jang HD, Rhee YW (2011) Sequential hydration with anaerobic and heat treatment increases GABA (γ-aminobutyric acid) content in wheat. Food Chem 129:1631–1635

    Article  CAS  Google Scholar 

  5. Park KB, Oh SH (2007) Production of yogurt with enhanced levels of γ-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Bioresour Technol 98:1675–1679

    Article  CAS  Google Scholar 

  6. Park SJ, Kim DH, Kang HJ, Shin MH, Yang SY, Yang JW, Jung YH (2021) Enhanced production of γ-aminobutyric acid (GABA) using Lactobacillus plantarum EJ2014 with simple medium composition. LWT Food Sci Technol 137:110443

    Article  CAS  Google Scholar 

  7. Kalueff A, Nutt DJ (1996) Role of GABA in memory and anxiety. Depress Anxiety 4:100–110

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M, Sansawa H (2003) Blood-pressure-lowering effect of a novel fermented milk containing gamma-aminobutyric acid (GABA) in mild hypertensives. Eur J Clin Nutr 57:490–495

    Article  CAS  Google Scholar 

  10. Li H, Cao Y (2010) Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39:1107–1116

    Article  CAS  Google Scholar 

  11. Wang L, Xu DX, Lv YG, Zhang H (2010) Purification and biochemical characterization of a novel glutamate decarboxylase from rice bran. J Sci Food Agric 90:1027–1033

    Article  CAS  Google Scholar 

  12. Oh SJ, Kim HS, Lim ST, Reddy CK (2019) Enhanced accumulation of gamma-aminobutyric acid in rice bran using anaerobic incubation with various additives. Food Chem 271:187–192

    Article  CAS  Google Scholar 

  13. Clark G, O’Mahony S, Malone G, Dinan TG (2007) An isocratic high performance liquid chromatography method for the determination of GABA and glutamate in discrete regions of the rodent brain. J Neurosci Methods 160:223–230

    Article  Google Scholar 

  14. Sawai Y, Yamaguchi Y, Miyama K, Yoshitomi H (2001) Cyclic treatment of anaerobic incubation increases the content of γ-aminobutyric acid in tea shoots. J Amino Acids 20:331–334

    Article  CAS  Google Scholar 

  15. Lee BJ, Kim JS, Mi KY, Lim JH, Kim MY, Lee SM, Jeong MH, Ahn CB, Je JY (2010) Antioxidant activity and γ-aminobutyric acid (GABA) content in sea tangle fermented by Lactobacillus brevis BJ20 isolated from traditional fermented foods. J Food Chem 122:271–276

    Article  CAS  Google Scholar 

  16. Mazur R, Kovalovska K, Hudecin J (2011) Change in selectivity of gamma-aminobutyric acid formation effected by fermentation condition and microorganisms. J Microbiol Biotechnol Food Sci 1:164–171

    CAS  Google Scholar 

  17. Roohinejad S, Mirhosseini H, Saari N, Mustafa S, Alias I, Hussin ASM, Hamid A, Manap MY (2009) Evaluation of GABA, crude protein and amino acid composition from different varieties of Malaysian’s brown rice. Aust J Crop Sci 3:184–190

    CAS  Google Scholar 

  18. Hayat A, Jahangir TM, Khuhawar MY, Alamgir M, Siddiqui AJ, Musharraf SG (2014) Simultaneous HPLC determination of gamma amino butyric acid (GABA) and lysine in selected Pakistani rice varieties by pre-column derivatization with 2-Hydroxynaphth aldehyde. J Cereal Sci 60:356–360

    Article  CAS  Google Scholar 

  19. Komatsuzaki N, Shima J, Kawamoto S, Momose H, Kimura T (2005) Production of gamma-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol 22:497–504

    Article  CAS  Google Scholar 

  20. Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M (2007) Synthesis of gamma-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol 73:7280–7290

    Article  Google Scholar 

  21. Yang SY, Lu FX, Lu ZX, Bie XM, Jiao Y, Sun LJ, Yu B (2008) Production of γ-aminobutyric acid by Streptococcus salivarius subsp. thermophilus Y2 under submerged fermentation. Amino Acids 34:473–478

    Article  CAS  Google Scholar 

  22. Wang Q, Liu X, Fu J, Wang S, Chen Y, Chang K, Li H (2018) Substrate sustained release-based high efficacy biosynthesis of GABA by Lactobacillus brevis NCL912. Microb Cell Fact 17:80–88

    Article  Google Scholar 

  23. Kook MC, Cho SC (2013) Production of GABA (gamma aminobutyric acid) by lactic acid bacteria. Korean J Food Sci Anim Resour 33:377–389

    Article  Google Scholar 

  24. Eamarjharn A, Theerakulkait C, Thanachasai S (2016) Effect of incubation time, buffer type and concentration on gamma-aminobutyric acid (GABA) production using Khao Dawk Mali 105 rice bran. Agric Nat Resour 50:80–84

    CAS  Google Scholar 

  25. Kook MC, Seo MJ, Cheigh CI, Pyun YR, Cho SC, Park H (2010) Enhanced production of γ-aminobutyric acid using rice bran extracts by Lactobacillus sakei B2–16. J Microbiol Biotechnol 20:763–766

    CAS  PubMed  Google Scholar 

  26. Yao C, Chou J, Wang T, Zhao H, Zhang B (2018) Pantothenic acid, vitamin C, and biotin play important roles in the growth of Lactobacillus helveticus. Front Microbiol 9:1194–1202

    Article  Google Scholar 

  27. Zhuang K, Jiang Y, Feng X, Li L, Dang F, Zhang W, Man C (2018) Transcriptomic response to GABA-producing Lactobacillus plantarum CGMCC 1.2437T induced by L-MSG. PLoS One 13:e0199021

  28. Villegas JM, Brown L, de Giori GS, Hebert EM (2016) Optimization of batch culture conditions for GABA production by Lactobacillus brevis CRL 1942.; isolated from quinoa sourdough. LWT-Food Sci Technol 67:22–26

    Article  CAS  Google Scholar 

  29. Park EJ, Garcia CV, Youn SJ, Park CD, Lee SP (2019) Fortification of γ-aminobutyric acid and bioactive compounds in Cucurbita moschata by novel two-step fermentation using Bacillus subtilis and Lactobacillus plantarum. LWT-Food Sci Technol 102:22–29

    Article  CAS  Google Scholar 

  30. Sanchart C, Watthanasakphuban N, Boonseng O, Nguyen TH, Haltrich D, Maneerat S (2018) Tuna condensate as a promising low-cost substrate for glutamic acid and GABA formation using Candida rugosa and Lactobacillus futsaii. Process Biochem 70:29–35

    Article  CAS  Google Scholar 

  31. Kwon SY, Garcia CV, Song YC, Lee SP (2016) GABA-enriched water dropwort produced by co-fermentation with Leuconostoc mesenteroides SM and Lactobacillus plantarum K154. LWT-Food Sci Technol 73:233–238

    Article  CAS  Google Scholar 

  32. Lim JS, Garcia C, Lee SP (2016) Optimized production of GABA and γ-PGA in a turmeric and roasted soybean mixture co-fermented by Bacillus subtilis and Lactobacillus plantarum. Food Sci Technol Res 22:209–217

    Article  CAS  Google Scholar 

  33. Cotter PD, Hill C (2003) Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453

    Article  CAS  Google Scholar 

  34. Cui Y, Miao K, Niyaphorn S, Qu X (2020) Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int J Mol Sci 21:995–1114

    Article  CAS  Google Scholar 

  35. Park SY, Lee JW, Lim SD (2014) The probiotic characteristics and GABA production of Lactobacillus plantarum K154 isolated from Kimchi. Food Sci Biotechnol 23:1951–1957

    Article  CAS  Google Scholar 

  36. Tajabadi N, Ebrahimpour A, Baradaran A, Rahim RA, Mahyudin NA, Manap MYA, Abu Bakar F, Saari N (2015) Optimization of gamma-aminobutyric acid production by Lactobacillus plantarum Tak-Apis362 from honeybees. Molecules 20:6654–6669

    Article  CAS  Google Scholar 

  37. Zarei F, Nateghi L, Eshaghi MR, Abadi MET (2018) Optimization of gamma-aminobutyric acid production in probiotics extracted from local dairy products in west region of Iran using MRS broth and whey protein media. Appl Food Biotechnol 5:233–242

    CAS  Google Scholar 

  38. Dover S, Halpern YS (1972) Control of the pathway of γ-aminobutyrate breakdown in Escherichia coli K-12. J Bacteriol 110:165–170

    Article  CAS  Google Scholar 

  39. Feehily C, O’Byrne CP, Karatzas KAG (2013) Functional γ-aminobutyrate shunt in Listeria monocytogenes: role in acid tolerance and succinate biosynthesis. Appl Environ Microb 79:74–80

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a research grant from Hankyong National University in the year of 2018.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chae Hun Ra.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, N.Y., Kim, SK. & Ra, C.H. Evaluation of gamma-aminobutyric acid (GABA) production by Lactobacillus plantarum using two-step fermentation. Bioprocess Biosyst Eng 44, 2099–2108 (2021). https://doi.org/10.1007/s00449-021-02586-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-021-02586-8

Keywords

Navigation