Production of gaba (γ - Aminobutyric acid) by microorganisms: a review

Radhika Dhakal, Vivek K Bajpai, Kwang-Hyun Baek, Radhika Dhakal, Vivek K Bajpai, Kwang-Hyun Baek

Abstract

GABA (γ-aminobutyric acid) is a four carbon non-protein amino acid that is widely distributed in plants, animals and microorganisms. As a metabolic product of plants and microorganisms produced by the decarboxylation of glutamic acid, GABA functions as an inhibitory neurotransmitter in the brain that directly affects the personality and the stress management. A wide range of traditional foods produced by microbial fermentation contain GABA, in which GABA is safe and eco-friendly, and also has the possibility of providing new health-benefited products enriched with GABA. Synthesis of GABA is catalyzed by glutamate decarboxylase, therefore, the optimal fermentation condition is mainly based on the biochemical properties of the enzyme. Major GABA producing microorganisms are lactic acid bacteria (LAB), which make food spoilage pathogens unable to grow and act as probiotics in the gastrointestinal tract. The major factors affecting the production of GABA by microbial fermentation are temperature, pH, fermentation time and different media additives, therefore, these factors are summarized to provide the most up-dated information for effective GABA synthesis. There has been a huge accumulation of knowledge on GABA application for human health accompanying with a demand on natural GABA supply. Only the GABA production by microorganisms can fulfill the demand with GABA-enriched health beneficial foods.

Keywords: GABA (γ -aminobutyric acid); GABA-enriched food.; lactic acid bacteria; microorganisms; optimal conditions.

Figures

Figure 1
Figure 1
Decarboxylation of L-glutamate to GABA by glutamate decarboxylase (GAD). PLP: pyridoxal-5’-phosphate.

References

    1. Adeghate E., Ponery A.S. GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats. Tissue Cell. 2002;34:1–6.
    1. Aoki H., Uda I., Tagami K., Furuya Y., Endo Y., Fujimoto K. The production of a new tempeh like fermented soybean containing a high level of γ- aminobutyric acid by anaerobic incubation with Rhizopus. Biocsi. Biotechnol. Biochem. 2003;67(5):1018–1023.
    1. Blanc P.J., Loret M.O., Santerre A.T., Pareilleux A., Prome D., Prome J.C., Laussac J.P., Goma G. Pigment of Monascus. J. Food Sci. 1994;59:862–865.
    1. Bloch-Tardy M., Roland B., Gonnard P. Pig brain 4-aminobutyrate 2-ketoglutarate transaminase. Purification, kinetics and physical properties. Biochimie. 1974;56:823–832.
    1. Capitani G.D.E., Biase D., Aurizi C., Gut H., Bossa F., Grutter M.G. Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J. 2003;22:4027–4037.
    1. Cash C., Maitre M., Ciesielski L., Mandel P. Purification and partial characterisation of 4- aminobutyrate 2-ketoglutarate transaminase from human brain. FEBS Lett. 1974;47:199–203.
    1. Castanie-Cornet M.P., Smith T.A.D., Elliott J.F., Foster J.W. Control of acid resistance in Escherichia coli. J. Bacteriol. 1999;181:3525–3535.
    1. Castor J.G.B. The B-complex vitamins of musts and wines as microbial growth factors. Appl. Microbiol. 1953;1:97–102.
    1. Chamba J.F., Irlinger F. Secondary and adjunct cultures. In: Fox P.F., McSweeney P.L.H., Cogan T.M., Guinee T.P., Cheese, editors. Chem. Phy. Microbiol. Elsevier. London, UK: 2004. pp. 191–206.
    1. Chembler J.A., Koffas M.A.G. Metabolic engeneering for plant natural product biosynthesis in microbes. Curr. Opin. Biotech. 2008;19:597–605.
    1. Chen K.N., Chen M.J., Liu J.R., Lin C.W., Chiu H.Y. Optimization of incorporated probiotics as coating materials for probiotic microencapsulation. J. Food Sci. 2004;70:260–266.
    1. Cho Y.R., Chang J.Y., Chang H.C. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 2007;17:104–109.
    1. Choi S.I., Lee J.W., Park S.M., Lee M.Y., Ge J.I., Park M.S., Heo T.R. Improvement of gamma-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 2006;16:562–568.
    1. Chou L.S., Weimer B. Isolation and characterization of acid and bile-tolerant isolates from strains of Lactobacillus acidophilus. J. Dairy Sci. 1999;82:23–31.
    1. Coda R., Rizzello C.G., Gobbetti M. Use of sourdough fermentation and pseudo-cereals and leguminous flours for the making of a functional bread enriched of γ-aminobutyric acid (GABA) Int. J. Food Microbiol. 2010;137:236–245.
    1. Cotter P.D., Hill. C. Surviving the acid text: responses of grampositive bacteria to low pH. Microbiol. Mol. Biol. Rev. 2003;67:429–453.
    1. Di Cagno R., Mazzacane F., Rizzello C.G., Angelis M.D.E., Giuliani G., Meloni M., Servi B.D.E., Marco G. Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl. Microbiol. Biotechnol. 2010;86:731–741.
    1. Djenane D., Martínez L., Blanco D., Yanguela J., Yanguela J.A., Roncales P. Effect of lactic acid bacteria on extention of shelf life and growth of listeria monocytogenes in beef steaks stored in co2-rich atmosphere. Braz. J. Microboil. 2005;36:405–412.
    1. Foester C.W., Foester H.F. Glutamic acid decarboxylase in spores of Bacillus megaterium and its possible involvement in spore germination. J. Bacteriol. 1973;114:1090–1098.
    1. Foester H.F. G-aminobutyric acid as a required germinant for mutant spores of Bacillus megaterium. J. Bacteriol. 1971:817–823.
    1. Franciosi E., Settanni L., Cavazza A., Poznanski E. Biodiversity and technological potential of wild lactic acid bacteria from raw cows’ milk. Int. Dairy J. 2009a;19:3–11.
    1. Hagiwara H., Seki T., Ariga T. The effect of pre-germinated brown rice intake on blood glucose and PAI-1 levels in streptozotocin-induced diabetic rats. Biosci. Biotechnol. Biochem. 2004;68:444–447.
    1. Han B.Z., Rombouts F.M., Robert Nout M.J. A Chinese fermented soybean food. Int. J. Food Microbiol. 2001;65:1–10.
    1. Hao R., Schmit J.C. Cloning of the gene for glutamate decarboxylase and its expression during conidiation in Neurospora crassa. Biochem. J. 1993;293:735–738.
    1. Hayakawa K., Ueno Y., Kawamura S., Taniguchi R., Oda K. Production of y-aminobutyric acid by lactic acid bacteria. Seibutsu Kogaku. 1997;75:239–244.
    1. Hayakawa K., Kimura M., Kasaha K., Matsumoto K., Sansawa H., Yamori Y. Effect of a γ-aminobutyric acid-enriched dairy product on the blood pressure of spontaneously hypertensive and normotensive Wistar–Kyoto rats. Bri. J. Nutr. 2004;92:411–417.
    1. Heck J.X., Hertz P.F., Ayub M.A.Z. Cellulase and xylanase production by isolated amazon Bacillus strains using soybean industrial residue based solid-state cultivation. Braz. J. Microbiol. 2002;33:213–218.
    1. Higuchi T., Hayashi H., Abe K. Exchange of glutamate and g-aminobutyrate in a Lactobacillus strain. J. Bacteriol. 1997;179:3362–3364.
    1. Holzapfel W.H., Geisen R., Schillinger U. Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Int. J. Food Microbiol. 1995;24:343–362.
    1. Huang J., Mei L., Wu H., Lin D. Biosynthesis of c-aminobutyric acid (GABA) using immobilized whole cells of Lactobacillus brevis. World J. Microbiol. Biotechnol. 2007;23:865–871.
    1. Huang J., Mei L., Sheng Q., Yao S., Lin D. Purification and characterization of glutamate decarboxylase of lactobacillus brevis CGMCC 1306 isolated from fresh milk. Chinese J. Chem. Eng. 2007;15:157–161.
    1. Huang J., Mei L., Xia J. Application of artificial neural network coupling particle swarm optimization algorithm to biocatalytic production of GABA. Biotechnol. Bioeng. 2007;96:924–931.
    1. Inoue K., Shirai T., Ochiai H., Kasao M., Hayakawa K., Kimura M., Sansawa H. Blood-pressure-lowering effect of a novel fermented milk containing γ-aminobutyric acid (GABA) in mild hypertensives. Eur. J. Clin. Nutr. 2003;57:490–495.
    1. Izquierdo E., Marchioni E., Aoude-Werner D., Hasselmann C., Ennahar S. Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes. Food Microbiol. 2009;26:16–20.
    1. Jakoby W.B., Scott E.M. Aldehyde oxidation. III. Succinic semialdehyde dehydrogenase. J. Biol. Chem. 1959;234(4):937–940.
    1. Jannoey P., Niamsup H., Lumyong S., Suzuki T., Katayama T., Chairote G. Comparison of gamma-aminobutyric acid production in Thai rice grains. World J. Microbiol. Biotechnol. 2010;26:257–263.
    1. Jeng K.C., Chen C.S., Fang Y.P., Hou R.C.W., Chen Y.S. Effect of microbial fermentation on content of statin, GABA, and polyphenols in Pu-Erh tea. J. Agric. Food Chem. 2007;55:8787–8792.
    1. Kim J.Y., Lee M.Y., Ji G.E., Lee Y.S., Hwang K.T. Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int. J. Food Microbiol. 2009;130:12–16.
    1. Kimura M., Hayakawa K., Sansawa H. Involvement of γ-aminobutyric acid (GABA) B receptors in the hypotensive effect of systemically administered GABA in spontaneously hypertensive rats. Jpn. J. Pharmacol. 2002;89:388–394.
    1. Kono I., Himeno K. Changes in g-aminobutyric acid content during beni-koji making. Biosci. Biotechnol. Biochem. 2000;64:617–619.
    1. Kubicek C.P., Hampel W., Rohr M. Manganese deficiency leads to elevated amino acid pools in critic acid accumulating Aspergillus niger. Arch. Microbiol. 1979;123:73–79.
    1. Kumar S., Punekar N.S., Satyanarayan V., Venkatesh K.V. Metabolic fate of glutamate and evaluation of flux through the 4–aminobutyrate (GABA) shunt in Aspergillus niger. Biotechnol. Bioeng. 2000;67:575–584.
    1. Komatsuzaki N., Shima J., Kawamotoa S., Momosed H., Kimurab T. Production of g-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 2005;22:497–504.
    1. Krishnaswamy P.R., Giri K.V. The occurrence of 4-aminobutyric acid and glutamic acid decarboxylase in red yeast (Rhodotorula glutinis) Curr. Sci. 1953;22:143–144.
    1. Lee B.J., Kim J.S., Kang Y.M., Lim J.H., Kim Y.M., Lee M.S., Jeong M.H., Ahn C.B., Je J.Y. Antioxidant activity and γ-aminobutyric acid (GABA) content in sea tangle fermented by Lactobacillus brevis BJ20 isolated from traditional fermented foods. Food Chem. 2010;122(1):271–276.
    1. Leroy F., Vuyst L.D. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 2004;15:67–78.
    1. Li H., Gao D., Cao Y., Xu H. A high γ-aminobutyric acid-producing Lactobacillus brevis isolated from Chinese traditional paocai. Ann. Microbiol. 2008;58(4):649–653.
    1. Li H., Cao Y. Lactic acid bacterial cell factories for gamma -aminobutyric acid. Amino Acids. 2010;39:1107–1116.
    1. Li H., Qiu T., Huang G., Cao Y. Production of gamma-aminobutyric acid by Lactobacillus brevis NCL912 using fed-batch fermentation. Microb. Cell Fact. 2010;9:85.
    1. Li H., Qiu T., Gao D., Cao Y. Medium optimization for production of gamma-aminobutyric acid by Lactobacillus brevis NCL912. Amino Acids. 2010;38:1439–1445.
    1. Li Q., Yao H.Y., Zhang H. Studies on Screening for γ-aminobutyric acid producer and optimization of fermentation conditions. Chin. J. Amino Acids Biotic Res. 2004;26(1):40–43.
    1. Lu X., Xie C., Gu Z. Isolation of γ-aminobutyric acid-producing bacteria and optimization of fermentative medium. Biochem. Eng. J. 2008;41:48–52.
    1. Lu X., Xie C., Gu Z. Optimisation of fermentative parameters for GABA enrichment by Lactococcus lactis. Czech. J. Food Sci. 2009;27(6):433–442.
    1. Maras B., Sweeney G., Barra D., Bossa F., John R.A. The amino acid sequence of glutamate decarboxylase from Escherichia coli. Eur. J. Biochem. 1992;204:93–98.
    1. Miura D., Ito Y., Mizukuchi A., Kise M., Aoto H., Yagasaki K. Hypercholesterolemic action of pre-germinated brown rice in hepatoma-bearing rats. Life Sci. 2006;79:259–264.
    1. Nikolaeva Z.K., Yu V.V. Mechanism of action of y-aminobutyrate-glutamate transaminase from pig kidney. Biokhimiya. 1972;37:572–578.
    1. Nishida S., Michinaka A., Nakashima K., Iino H., Fujii T. 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. 2008;54:267–276.
    1. Nomura M., Kimoto H., Someya Y., Furukawa S., Suzuki I. Production of gamma-aminobutyric acid by cheese starters during cheese ripening. J. Dairy Sci. 1998;81:1486–1491.
    1. 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. 2000;47:596–603.
    1. Park K.B., Oh S.H. Isolation and characterization of Lactobacillus buchneri strains with high gamma-aminobutyric acid producing capacity from naturally aged cheese. Food Sci. Biotechnol. 2006b;15:86–90.
    1. 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. 2007;98:1675–1679.
    1. Pimentel M.C.B., Melo E.H.M., Filho J.L.L. DURAN N. Production of lipase free of citrinin by Penicillium citrinum. Mycopathologia. 1996;133:119–121.
    1. Plokhov A.Y., Gusyatiner M.M., Yampolskaya T.A., Kaluzhsky V.E., Sukhareva B.S., Schulga A.A. Preparation of gamma-aminobutyric acid using E. coli cells with high activity of glutamate decarboxylase. Appl. Biochem. Biotechnol. 2000;88:257–265.
    1. Reed L.J. The occurrence of c-aminobutyric acid in yeast extract; its isolation and identification. J. Biol. Chem. 1950;183:451–458.
    1. Rizzello C.G., Cassone A., Cagno R.DI., Gobbetti M. Synthesis of Angiotensin I-Converting Enzyme (ACE)-Inhibitory peptides and γ-aminobutyric acid (GABA) during sourdough fermentation by selected lactic acid bacteria. J. Agric. Food Chem. 2008;56:6936–6943.
    1. Saikusa T., Horino T., Mori Y. Accumulation of g-aminobutyric acid (Gaba) in the rice germ during water soaking. Biosci. Biotech. Biochem. 1994;58:2291–2292.
    1. Sanders J.W., Leenhouts K., Burghoorn J., Brands J.R., Venema G., Kok J. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol. Microbiol. 1998;27:299–310.
    1. Sandmeier E., Hale T.I., Christen P. Multiple evolutionary origin of pyridoxal 50-phosphate-dependent amino acid decarboxylase. Eur. J. Biochem. 1994;221:997–1002.
    1. Sawai Y., Yamaguchi Y., Miyana D., Yoshitomi H. Cycling treatment of anaerobic and aerobic incubation increases the content of g-aminobutyric acid in tea shoots. Amino Acids. 2001;20:331–334.
    1. Schmit J.C., Brody S. Neurospora crassa conidial germination: role of endogenous amino acid pools. J. Bacteriol. 1975;124:232–242.
    1. Scott E.M., Jakoby W.B. Soluble y-aminobutyric- glutamic transaminase from Pseudomonas fluorescens. J. Biol. Chem. 1959;234:932–936.
    1. Servili M., Rizzello C.G., Taticchi A., Esposto S., Urbani S., Mazzacane F., Di Maio I., Selvaggini R., Gobbetti M., Di Cagno R. Functional milk beverage fortified with phenolic compounds extracted from olive vegetation water, and fermented with functional lactic acid bacteria. Int. J. Food Microbiol. 2011;147(1):45–52.
    1. Settanni L., Corsetti A. Application of bacteriocins in vegetable food biopreservation. Int. J. Food Microbiol. 2008;121:123–138.
    1. Seok J.H., Park K.B., Kim Y.H., Bae M.O., Lee M.K., Oh S.H. Production and characterization of kimchi with enhanced levels of gamma-aminobutyric acid. Food Sci. Biotechnol. 2008;17:940–946.
    1. Shelp B.J., Bown A.W., Mclean M.D. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 1999;4:446–452.
    1. Siragusa S., Angelis ., Cagno R.Di., Rizzello C.G., Coda R., Gobbetti M. Appl. Environ. Microbiol. 2007. Synthesis of γ -aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses; pp. 7283–7290.
    1. Skeie S., Lindberg C., Narvhus J. Development of amino acids and organic acids in Norvegia, influence of milk treatment and adjunct Lactobacillus. Int. Dairy J. 2001;11:399–411.
    1. Smith D.K., Kassam T., Singh B., Elliott J.F. Escherichia coli has two homologousglutamate decarboxylase genes that map to distinct loci. J. Bacteriol. 1992;174:5820–5826.
    1. Soo I.M.C., Lee J.W., Park S.M., Lee M.Y., Ji G.E., Park M.S., Heo T.R. Improvement of γ-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 2006;16(4):562–568.
    1. Steward F.C., Thompson J.F., Dent C.E. γ- aminobutyric acid: a constituent of the potato tuber? Science. 1949;110:439–440.
    1. Su Y.C., Wang J.J., Lin T.T., Pan T.M. Production of the secondary metabolites gamma-aminobutyric acid and monacolin K by Monascus. J. Ind. Microbiol. Biotechnol. 2003;30:41–46.
    1. Sun B.S., Zhou L.P., Jia X.Q., Sung C.K. Response surface modeling for g-aminobutyric acid production by Monascus pilosus GM100 under solid-state fermentation. Afr. J. Biotechnol. 2008;7(24):4544–4550.
    1. Tsai J.S., Lin Y.S., Pan B.S., Chen T.J. Antihypertensive peptides and gamma-aminobutyric acid from prozyme 6 facilitated lactic acid bacteria fermentation of soymilk. Process Biochem. 2006;41:1282–1288.
    1. Tsushida T., Murai T. Conversion of glutamic acid to g-aminobutyric acid in tea leaves under anaerobic conditions. Agric. Biol. Chem. 1987;51:2865–2871.
    1. Ueno H. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B: Enzym. 2000;10:67–79.
    1. Ueno Y., Hayakawa K., Takahashi S., Oda K. Purification and characterization of glutamate decarboxylase from Lactobacillus brevis IFO 12005. Biosci. Biotech. Biochem. 1997;61:1168–1171.
    1. Voellmy R., Leisinger T. Role of 4-aminobutyrate aminotransferase in the arginine metabolism of Pseudomonas aeruginosa. J. Bacteriol. 1976;128(3):722–729.
    1. Wang J.J., Lee C.L., Pan T.M. Improvement of monacolin K, c-aminobutyric acid and citrinin production ratio as a function of environmental conditions of Monascus purpureus NTU 601. J. Ind. Microbiol. Biotechnol. 2003;30:669–676.
    1. Wouters J.T.M., Ayad E.H., Hugenholtz J., Smit G. Microbes from raw milk for fermented dairy products. Int. Dairy J. 2002;12:91–109.
    1. Yang S.Y., Lu F.X., Lu Z.X., Bie X.M., Jiao Y., Sun L.J., Yu B. Production of gamma-aminobutyric acid by Streptococcus salivarius subsp thermophilus Y2 under submerged fermentation. Amino Acids. 2008;34:473–478.
    1. Yokoyama S., Hiramatsu J., Hayakawa K. Production of y-aminobutyric acid from alcohol distillery lees by Lactobacilus brevis IFO- 12005. J. Biosci. Bioeng. 2002;93(1):95–97.

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa