Abstract
Gamma-aminobutyric acid is a non-protein amino acid that is widely present in organisms. Several important physiological functions of gamma-aminobutyric acid have been characterized, such as neurotransmission, induction of hypotension, diuretic effects, and tranquilizer effects. Many microorganisms can produce gamma-aminobutyric acid including bacteria, fungi and yeasts. Among them, gamma-aminobutyric acid-producing lactic acid bacteria have been a focus of research in recent years, because lactic acid bacteria possess special physiological activities and are generally regarded as safe. They have been extensively used in food industry. The production of lactic acid bacterial gamma-aminobutyric acid is safe and eco-friendly, and this provides the possibility of production of new naturally fermented health-oriented products enriched in gamma-aminobutyric acid. The gamma-aminobutyric acid-producing species of lactic acid bacteria and their isolation sources, the methods for screening of the strains and increasing their production, the enzymatic properties of glutamate decarboxylases and the relative fundamental research are reviewed in this article. And the potential applications of gamma-aminobutyric acid-producing lactic acid bacteria were also referred to.
Similar content being viewed by others
References
Abe Y, Umemura S, Sugimoto K, Hirawa N, Kato Y, Yokoyama N, Yokoyama T, Iwai J, Ishii M (1995) Effect of green tea rich in gamma-aminobutyric acid on blood pressure of Dahl salt-sensitive rats. Am J Hypertens 8:74–79
Adeghate E, Ponery AS (2002) GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats. Tissue Cell 34:1–6
Aoki H, Furuya Y, Endo Y, Fujimoto K (2003) Effect of gamma-aminobutyric acid-enriched tempeh-like fermented soybean (GABA-tempeh) on the blood pressure of spontaneously hypertensive rats. Biosci Biotechnol Biochem 67:1806–1808
Ben Omar N, Ampe F, Raimbault M, Guyot JP, Tailliez P (2000) Molecular diversity of lactic acid bacteria from cassava sour starch (Colombia). Syst Appl Microbiol 23:285–291
Capitani G, De Biase D, Aurizi C, Gut H, Bossa F, Grutter MG (2003) Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J 22:4027–4037
Cho YR, Chang JY, Chang HC (2007) Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol 17:104–109
Choi SI, Lee JW, Park SM, Lee MY, Ji GE, Park MS, Heo TR (2006) Improvement of gamma-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J Microbiol Biotechnol 16:562–568
Chou LS, Weimer B (1999) Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. J Dairy Sci 82:23–31
Di Cagno R, Mazzacane F, Rizzello CG, De Angelis M, Giuliani G, Meloni M, De Servi B, Gobbetti M (2010) Synthesis of gamma-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl Microbiol Biotechnol 86:731–741
Gardner NJ, Savard T, Obermeier P, Caldwell G, Champagne CP (2001) Selection and characterization of mixed starter cultures for lactic acid fermentation of carrot, cabbage, beet and onion vegetable mixtures. Int J Food Microbiol 64:261–275
Hagiwara H, Seki T, Ariga T (2004) The effect of pre-germinated brown rice intake on blood glucose and PAI-1 levels in streptozotocin-induced diabetic rats. Biosci Biotechnol Biochem 68:444–447
Hayakawa K, Kimura M, Kasaha K, Matsumoto K, Sansawa H, Yamori Y (2004) Effect of a gamma-aminobutyric acid-enriched dairy product on the blood pressure of spontaneously hypertensive and normotensive Wistar–Kyoto rats. Br J Nutr 92:411–417
Higuchi T, Hayashi H, Abe K (1997) Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. J Bacteriol 179:3362–3364
Hiraga K, Ueno Y, Oda K (2008) Glutamate decarboxylase from Lactobacillus brevis: activation by ammonium sulfate. Biosci Biotechnol Biochem 72:1299–1306
Horie H, Rechnitz GA (1995) Enzymatic flow-injection determination of gamma-aminobutyric-acid. Anal Lett 28:259–266
Huang J, Mei L, Sheng Q, Yao S, Lin D (2007a) Purification and characterization of glutamate decarboxylase of Lactobacillus brevis CGMCC 1306 isolated from fresh milk. Chinese J Chem Eng 15:157–161
Huang J, Mei L, Wu H, Lin D (2007b) Biosynthesis of γ-aminobutyric acid (GABA) using immobilized whole cells of Lactobacillus brevis. World J Microbiol Biotechnol 23:865–871
Hwanhlem N, Watthanasakphuban N, Riebroy S, Benjakul S, H-Kittikun A, Maneerat S (2010) Probiotic lactic acid bacteria from Kung-Som: isolation, screening, inhibition of pathogenic bacteria. Intel J Food Sci Technol 45:594–601
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
Jakobs C, Jaeken J, Gibson KM (1993) Inherited disorders of GABA metabolism. J Inherit Metab Dis 16:704–715
Junter GA, Jouenne T (2004) Immobilized viable microbial cells: from the process to the proteome… or the cart before the horse. Biotechnol Adv 22:633–658
Kagan IA, Coe BL, Smith LL, Huo CJ, Dougherty CT, Strickland JR (2008) A validated method for gas chromatographic analysis of gamma-aminobutyric acid in tall fescue herbage. J Agric Food Chem 56:5538–5543
Karahan AG, Kilic GB, Kart A, Aloglu HS, Oner Z, Aydemir S, Erkus O, Harsa S (2010) Genotypic identification of some lactic acid bacteria by amplified fragment length polymorphism analysis and investigation of their potential usage as starter culture combinations in Beyaz cheese manufacture. J Dairy Sci 93:1–11
Kim SH, Shin BH, Kim YH, Nam SW, Jeon SJ (2007) Cloning and expression of a full-length glutamate decarboxylase gene from Lactobacillus brevis BH2. Biotechnol Bioprocess Eng 12:707–712
Kim JY, Lee MY, Ji GE, Lee YS, Hwang KT (2009) Production of gamma-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int J Food Microbiol 130:12–16
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
Komatsuzaki N, Nakamura T, Kimura T, Shima J (2008) Characterization of glutamate decarboxylase from a high gamma-aminobutyric acid (GABA)-producer, Lactobacillus paracasei. Biosci Biotechnol Biochem 72:278–285
Kono I, Himeno K (2000) Changes in gamma-aminobutyric acid content during beni-koji making. Biosci Biotechnol Biochem 64:617–619
Lee JY, Kim CJ, Kunz B (2006) Identification of lactic acid bacteria isolated from kimchi and studies on their suitability for application of as starter culture in the production fermented sausages. Meat Sci 72:437–445
Leroy F, Vuyst LD (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78
Li H, Cao Y, Gao D, Xu H (2008) A high γ-aminobutyric acid-producing ability Lactobacillus brevis isolated from Chinese traditional paocai. Ann Microbiol 58:649–653
Li H, Qiu T, Cao Y, Yang J, Huang Z (2009a) Pre-staining paper chromatography method for quantification of gamma-aminobutyric acid. J Chromatogr A 1216:5057–5060
Li H, Qiu T, Gao D, Cao Y (2009b) Medium optimization for production of gamma-aminobutyric acid by Lactobacillus brevis NCL912. Amino Acids. doi:10.1007/s00726-009-0355-3
Lu X, Chen Z, Gu Z, Han Y (2008) Isolation of gamma-aminobutyric acid-producing bacteria and optimization of fermentative medium. Biochem Eng J 41:48–52
Lu X, Xie C, Gu Z (2009) Optimisation of fermentative parameters for GABA enrichment by Lactococcus lactis. Czech J Food Sci 27:433–442
Masuda K, Guo XF, Uryu N, Hagiwara T, Watabe S (2008) Isolation of marine yeasts collected from the Pacific Ocean showing a high production of gamma-aminobutyric acid. Biosci Biotechnol Biochem 72:3265–3272
Nagaoka H (2005) Treatment of germinated wheat to increase levels of GABA and IP6 catalyzed by endogenous enzymes. Biotechnol Prog 21:405–410
Nishida S, Michinaka A, Nakashima K, Iino H, Fujii T (2008) Evaluation of the probiotic potential of Lactobacillus paracasei KW3110 based on in vitro tests and oral administration tests in healthy adults. J Gen Appl Microbiol 54:267–276
Nomura M, Kimoto H, Someya Y, Furukawa S, Suzuki I (1998) Production of gamma-aminobutyric acid by cheese starters during cheese ripening. J Dairy Sci 81:1486–1491
Nomura M, Kimoto H, Someya Y, Suzuki I (1999a) Novel characteristic for distinguishing Lactococcus lactis subsp. lactis from subsp. cremoris. Int J Syst Bacteriol 49:163–166
Nomura M, Nakajima I, Fujita Y, Kobayashi M, Kimoto H, Suzuki I, Aso H (1999b) Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145:1375–1380
Nomura M, Kobayashi M, Ohmomo S, Okamoto T (2000) Inactivation of the glutamate decarboxylase gene in Lactococcus lactis subsp. cremoris. Appl Environ Microbiol 66:2235–2237
Oh SH (2003) Stimulation of gamma-aminobutyric acid synthesis activity in brown rice by a chitosan/glutamic acid germination solution and calcium/calmodulin. J Biochem Mol Biol 36:319–325
Park KB, Oh SH (2004) Cloning and expression of a full-length glutamate decarboxylase gene from Lactobacillus plantarum. J Food Sci Nutr 9:324–329
Park KB, Oh SH (2005) Production and characterization of GABA rice yogurt. Food Sci Biotech 14:518–522
Park KB, Oh SH (2006a) Enhancement of gamma-aminobutyric acid production in Chungkukjang by applying a Bacillus subtilis strain expressing glutamate decarboxylase from Lactobacillus brevis. Biotechnol Lett 28:1459–1463
Park KB, Oh SH (2006b) Isolation and characterization of Lactobacillus buchneri strains with high gamma-aminobutyric acid producing capacity from naturally aged cheese. Food Sci Biotechnol 15:86–90
Park KB, Oh SH (2006c) Isolation and characterization of Lactobacillus buchneri strains with high gamma-aminobutyric acid producing capacity from naturally aged cheese. Food Sci Biotechnol 15:86–90
Park KB, Oh SH (2007a) Cloning, sequencing and expression of a novel glutamate decarboxylase gene from a newly isolated lactic acid bacterium, Lactobacillus brevis OPK-3. Bioresour Technol 98:312–319
Park KB, Oh SH (2007b) Production of yogurt with enhanced levels of gamma-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Bioresour Technol 98:1675–1679
Rhyu MR, Kim EY, Kim HY, Ahn BH, Yang CB (2000) Characteristics of the red rice fermented with fungus Monascus. Food Sci Biotechnol 9:21–26
Rizzello CG, Cassone A, Di Cagno R, Gobbetti M (2008) Synthesis of angiotensin I-converting enzyme (ACE)-inhibitory peptides and gamma-aminobutyric acid (GABA) during sourdough fermentation by selected lactic acid bacteria. J Agric Food Chem 56:6936–6943
Rossetti V, Lombard A (1996) Determination of glutamate decarboxylase by high-performance liquid chromatography. J Chromatogr B 681:63–67
Sanders JW, Leenhouts K, Burghoorn J, Brands JR, Venema G, Kok J (1998) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol 27:299–310
Satokari RM, Vaughan EE, Smidt H, Saarela M, Matto J, de Vos WM (2003) Molecular approaches for the detection and identification of bifidobacteria and lactobacilli in the human gastrointestinal tract. Syst Appl Microbiol 26:572–584
Schuller HM, Al-Wadei HAN, Majidi M (2008) Gamma-aminobutyric acid, a potential tumor suppressor for small airway-derived lung adenocarcinoma. Carcinogenesis 29:1979–1985
Seidl R, Cairns N, Singewald N, Kaehler ST, Lubec G (2001) Differences between GABA levels in Alzheimer’s disease and Down syndrome with Alzheimer-like neuropathology. Naunyn-Schmiedeberg’s Arch Pharmacol 363:139–145
Seok JH, Park KB, Kim YH, Bae MO, Lee MK, Oh SH (2008) Production and characterization of kimchi with enhanced levels of gamma-aminobutyric acid. Food Sci Biotechnol 17:940–946
Sethi ML (1999) Enzyme inhibition XI: glutamate decarboxylase activity relationship with the reaction products as determined by the colorimetric and radioisotopic methods. J Pharm Biomed Anal 19:847–854
Shizuka F, Kido Y, Nakazawa T, Kitajima H, Aizawa C, Kayamura H, Ichijo N (2004) Antihypertensive effect of gamma-amino butyric acid enriched soy products in spontaneously hypertensive rats. Biofactors 22:165–167
Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M (2007) Synthesis of γ-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol 73:7283–7290
Skeie S, Lindberg C, Narvhus J (2001) Development of amino acids and organic acids in Norvegia, influence of milk treatment and adjunct Lactobacillus. Inter Dairy J 11:399–411
Small PL, Waterman SR (1998) Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli. Trends Microbiol 6:214–216
Song Y, Shenwu M, Dhossche DM, Liu YM (2005) A capillary liquid chromatographic/tandem mass spectrometric method for the quantification of gamma-aminobutyric acid in human plasma and cerebrospinal fluid. J Chromatogr B 814:295–302
Su YC, Wang JJ, Lin TT, Pan TM (2003) Production of the secondary metabolites gamma-aminobutyric acid and monacolin K by Monascus. J Ind Microbiol Biotechnol 30:41–46
Sun TS, Zhao SP, Wang HK, Cai CK, Chen YF, Zhang HP (2009) ACE-inhibitory activity and gamma-aminobutyric acid content of fermented skim milk by Lactobacillus helveticus isolated from Xinjiang koumiss in China. Eur Food Res Technol 228:607–612
Svensson E, Skoog A, Amend JP (2004) Concentration and distribution of dissolved amino acids in a shallow hydrothermal system, Vulcano Island (Italy). Org Geochem 35:1001–1014
Tannock GW (2004) A special fondness for lactobacilli. Appl Environ Microbiol 70:3189–3194
Tsai JS, Lin YS, Pan BS, Chen TJ (2006) Antihypertensive peptides and gamma-aminobutyric acid from prozyme 6 facilitated lactic acid bacteria fermentation of soymilk. Process Biochem 41:1282–1288
Tsukatani T, Higuchi T, Matsumoto K (2005) Enzyme-based microtiter plate assay for gamma-aminobutyric acid: application to the screening of gamma-aminobutyric acid-producing lactic acid bacteria. Anal Chim Acta 540:293–297
Tsushida T, Murai T (1987) Conversion of glutamic-acid to gamma-aminobutyric-acid in tea leaves under anaerobic conditions. Agric Biol Chem 51:2865–2871
Tujioka K, Ohsumi M, Horie K, Kim M, Hayase K, Yokogoshi H (2009) Dietary gamma-aminobutyric acid affects the brain protein synthesis rate in ovariectomized female rats. J Nutr Sci Vitaminol 55:75–80
Tuohy KM, Probert HM, Smejkal CW, Gibson GR (2003) Using probiotics and prebiotics to improve gut health. Drug Discov Today 8:692–700
Ueno H (2000) Enzymatic and structural aspects on glutamate decarboxylase. J Mol Catal B Enzyme 10:67–79
Ueno Y, Hayakawa K, Takahashi S, Oda K (1997) Purification and characterization of glutamate decarboxylase from Lactobacillus brevis IFO 12005. Biosci Biotechnol Biochem 61:1168–1171
Wong CG, Bottiglieri T, Snead OC 3rd (2003) GABA, gamma-hydroxybutyric acid, and neurological disease. Ann Neurol 54:S3–12
Yan PM, Xue WT, Tan SS, Zhang H, Chang XH (2008) Effect of inoculating lactic acid bacteria starter cultures on the nitrite concentration of fermenting Chinese paocai. Food Control 19:50–55
Yang SY, Lu ZX, Lu FX, Bie XM, Sun LJ, Zeng XX (2006) A simple method for rapid screening of bacteria with glutamate decarboxylase activities. J Rapid Methods Autom Microbiol 14:291–298
Yang SY, Lu FX, Lu ZX, Bie XM, Jiao Y, Sun LJ, Yu B (2008) Production of gamma-aminobutyric acid by Streptococcus salivarius subsp thermophilus Y2 under submerged fermentation. Amino Acids 34:473–478
Yokoyama S, Hiramatsu J, Hayakawa K (2002) Production of gamma-aminobutyric acid from alcohol distillery lees by Lactobacillus brevis IFO-12005. J Biosci Bioeng 93:95–97
Zhang H, Yao HY, Chen F (2006) Accumulation of gamma-aminobutyric acid in rice germ using protease. Biosci Biotechnol Biochem 70:1160–1165
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, H., Cao, Y. Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39, 1107–1116 (2010). https://doi.org/10.1007/s00726-010-0582-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-010-0582-7