Production of GABA (γ-aminobutyric acid) by microorganisms: A review

Brazilian Journal of Microbiology

Volumn 43, Issue 4, 2012, Pages 1230-1241

  Dhakal, Radhika ^a   Bajpai, Vivek K ^a   Baek, Kwang Hyun ^a  

^a Yeungnam University   (South Korea)

Author keywords

GABA ( aminobutyric acid); GABA enriched food; Lactic acid bacteria; Microorganisms; Optimal conditions

Indexed keywords

EID: 84874374148     PISSN: 15178382     EISSN: 16784405     Source Type: Journal    
DOI: 10.1590/S1517-83822012000400001     Document Type: Article

References (91)

1. Adeghate, E.; Ponery, A.S. (2002). GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats. Tissue Cell 34, 1-6.
2. Aoki, H.; Uda, I.; Tagami, K.; Furuya, Y.; Endo, Y.; Fujimoto, K. (2003). 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. 67(5), 1018-1023.
3. Blanc, P.J.; Loret, M.O.; Santerre, A.T.; Pareilleux, A.; Prome, D.; Prome, J.C.; Laussac, J.P.; Goma, G. (1994). Pigment of Monascus. J. Food Sci. 59, 862-865.
4. Bloch-Tardy, M.; Roland, B.; Gonnard, P. (1974). Pig brain 4-aminobutyrate 2-ketoglutarate transaminase. Purification, kinetics and physical properties. Biochimie 56, 823-832.
5. Capitani, G.D.E.; Biase, D.; Aurizi, C.; Gut, H.; Bossa, F.; Grutter, M.G. (2003). Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J. 22, 4027-4037.
6. Cash, C.; Maitre, M.; Ciesielski, L.; Mandel, P. (1974). Purification and partial characterisation of 4-aminobutyrate 2-ketoglutarate transaminase from human brain. FEBS Lett. 47, 199-203.
7. Castanie-Cornet, M. P.; Smith, T. A. D.; Elliott, J. F.; Foster, J. W. (1999). Control of acid resistance in Escherichia coli. J. Bacteriol. 181, 3525-3535.
8. Castor, J.G.B. (1953). The B-complex vitamins of musts and wines as microbial growth factors. Appl. Microbiol. 1, 97-102.
9. Chamba, J.F.; Irlinger, F. (2004). Secondary and adjunct cultures. In: Fox, P.F., McSweeney, P.L.H., Cogan, T.M., Guinee, T.P. (Eds.), Cheese: Chem. Phy. Microbiol. Elsevier, London, UK, p. 191-206.
10. Chembler, J.A.; Koffas, M.A.G. (2008). Metabolic engeneering for plant natural product biosynthesis in microbes. Curr. Opin. Biotech. 19, 597-605.
11. Chen, K. N.; Chen, M. J.; Liu, J. R.; Lin, C. W.; Chiu, H. Y. (2004). Optimization of incorporated probiotics as coating materials for probiotic microencapsulation. J. Food Sci. 70, 260-266.
12. Cho, Y.R., Chang, J.Y., Chang, H.C. (2007). Production of gammaaminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 17, 104-109.
13. Choi, S.I.; Lee, J.W.; Park, S.M.; Lee, M.Y.; Ge J.I.; Park, M.S.; Heo, T.R. (2006). Improvement of gamma-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 16, 562-568.
14. Chou, L.S., Weimer, B. (1999). Isolation and characterization of acid and bile-tolerant isolates from strains of Lactobacillus acidophilus. J. Dairy Sci. 82, 23-31.
15. Coda, R.; Rizzello, C.G.; Gobbetti, M. (2010). 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. 137, 236-245.
16. Cotter, P. D.; C. Hill. (2003). Surviving the acid text: responses of grampositive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67, 429-453.
17. Di Cagno, R.; Mazzacane, F.; Rizzello, C.G.; Angelis, M.D.E.; Giuliani, G.; Meloni, M.; Servi, B.D.E.; Marco, G. (2010). Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl. Microbiol. Biotechnol. 86, 731-741.
18. Djenane, D.; Martínez, L.; Blanco, D.; Yanguela, J., Yanguela, J.A.; Roncales, P. (2005). 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. 36, 405-412.
19. Foester, C. W.; Foester, H. F. (1973). Glutamic acid decarboxylase in spores of Bacillus megaterium and its possible involvement in spore germination. J. Bacteriol. 114, 1090-1098.
20. Foester, H.F. (1971). G-aminobutyric acid as a required germinant for mutant spores of Bacillus megaterium. J. Bacteriol. 817-823.
21. Franciosi E.; Settanni L.; Cavazza A.; Poznanski E. (2009a). Biodiversity and technological potential of wild lactic acid bacteria from raw cows' milk. Int. Dairy J. 19, 3-11.
22. Hagiwara, H.; Seki, T.; Ariga, T. (2004). The effect of pre-germinated brown rice intake on blood glucose and PAI-1 levels in streptozotocininduced diabetic rats. Biosci. Biotechnol. Biochem. 68, 444-447.
23. Han B.Z.; Rombouts, F.M.; Robert Nout, M.J. (2001). A Chinese fermented soybean food. Int. J. Food Microbiol. 65, 1-10.
24. Hao R.; Schmit J.C. (1993). Cloning of the gene for glutamate decarboxylase and its expression during conidiation in Neurospora crassa. Biochem. J. 293, 735-738.
25. Hayakawa K.; Ueno Y.; Kawamura S.; Taniguchi R.; Oda K. (1997). Production of y-aminobutyric acid by lactic acid bacteria. Seibutsu Kogaku 75, 239-244.
26. Hayakawa, K.; Kimura, M.; Kasaha, K.; Matsumoto, K.; Sansawa, H.; Yamori, Y. (2004). Effect of a γ-aminobutyric acid-enriched dairy product on the blood pressure of spontaneously hypertensive and normotensive Wistar-Kyoto rats. Bri. J. Nutr. 92, 411-417.
27. Heck J.X.; Hertz P.F.; Ayub M.A.Z. (2002). Cellulase and xylanase production by isolated amazon Bacillus strains using soybean industrial residue based solid-state cultivation. Braz. J. Microbiol. 33, 213-218.
28. Higuchi, T.; Hayashi, H.; Abe, K. (1997). Exchange of glutamate and gaminobutyrate in a Lactobacillus strain. J. Bacteriol. 179, 3362-3364.
29. Holzapfel, W.H.; Geisen, R.; Schillinger, U. (1995). Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Int. J. Food Microbiol. 24, 343-362.
30. Huang, J.; Mei, L.; Wu, H.; Lin, D. (2007). Biosynthesis of caminobutyric acid (GABA) using immobilized whole cells of Lactobacillus brevis. World J. Microbiol. Biotechnol. 23, 865-871.
31. Huang, J.; Mei, L.; Sheng, Q.; Yao, S.; Lin, D. (2007). Purification and characterization of glutamate decarboxylase of lactobacillus brevis CGMCC 1306 isolated from fresh milk. Chinese J. Chem. Eng. 15, 157-161.
32. Huang, J.; Mei, L.; Xia, J. (2007). Application of artificial neural network coupling particle swarm optimization algorithm to biocatalytic production of GABA. Biotechnol. Bioeng. 96, 924-931.
33. 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 γ-aminobutyric acid (GABA) in mild hypertensives. Eur. J. Clin. Nutr. 57.490-495.
34. Izquierdo, E.; Marchioni, E.; Aoude-Werner, D.; Hasselmann, C.; Ennahar, S. (2009). Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes. Food Microbiol. 26, 16-20.
35. Jakoby, W.B.; Scott, E.M. (1959). Aldehyde oxidation. III. Succinic semialdehyde dehydrogenase. J. Biol. Chem. 234(4), 937-940.
36. Jannoey, P.; Niamsup, H.; Lumyong, S.; Suzuki, T.; Katayama, T.; Chairote, G. (2010). Comparison of gamma-aminobutyric acid production in Thai rice grains. World J. Microbiol. Biotechnol. 26, 257-263.
37. Jeng, K.C.; Chen, C.S.; Fang, Y.P.; Hou, R.C.W.; Chen, Y.S. (2007). Effect of microbial fermentation on content of statin, GABA, and polyphenols in Pu-Erh tea. J. Agric. Food Chem. 55, 8787-8792.
38. Kim, J.Y.; Lee, M.Y.; Ji, G.E.; Lee, Y.S.; Hwang, K.T. (2009). Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int. J. Food Microbiol. 130, 12-16.
39. Kimura, M.; Hayakawa, K.; Sansawa, H. (2002). Involvement of γ-aminobutyric acid (GABA) B receptors in the hypotensive effect of systemically administered GABA in spontaneously hypertensive rats. Jpn. J. Pharmacol. 89, 388-394.
40. Kono, I.; Himeno, K. (2000). Changes in g-aminobutyric acid content during beni-koji making. Biosci. Biotechnol. Biochem. 64, 617-619.
41. Kubicek, C. P.; Hampel W.; Rohr M. (1979). Manganese deficiency leads to elevated amino acid pools in critic acid accumulating Aspergillus niger. Arch. Microbiol. 123, 73-79.
42. Kumar, S.; Punekar, N.S.; Satyanarayan, V.; Venkatesh, K.V. (2000). Metabolic fate of glutamate and evaluation of flux through the 4- aminobutyrate (GABA) shunt in Aspergillus niger. Biotechnol. Bioeng. 67, 575-584.
43. Komatsuzaki, N.; Shima, J.; Kawamotoa, S.; Momosed, H.; Kimurab, T. (2005). Production of g-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22, 497-504.
44. Krishnaswamy, P. R.; Giri, K. V. (1953). The occurrence of 4-aminobutyric acid and glutamic acid decarboxylase in red yeast (Rhodotorula glutinis). Curr. Sci. 22, 143-144.
45. 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. (2010). Antioxidant activity and γ-aminobutyric acid (GABA) content in sea tangle fermented by Lactobacillus brevis BJ20 isolated from traditional fermented foods. Food Chem. 122 (1), 271-276.
46. Leroy, F.; Vuyst, L.D. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15, 67-78.
47. Li, H.; Gao, D.; Cao, Y.; Xu, H. (2008). A high γ-aminobutyric acidproducing Lactobacillus brevis isolated from Chinese traditional paocai. Ann. Microbiol. 58 (4), 649-653.
48. Li, H.; Cao, Y. (2010). Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39, 1107-1116.
49. Li, H.; Qiu, T.; Huang, G.; Cao, Y. (2010). Production of gammaaminobutyric acid by Lactobacillus brevis NCL912 using fed-batch fermentation. Microb. Cell Fact. 9, 85.
50. Li, H.; Qiu, T.; Gao, D.; Cao, Y. (2010). Medium optimization for production of gamma-aminobutyric acid by Lactobacillus brevis NCL912. Amino Acids 38, 1439-1445.
51. Li, Q.; Yao, H.Y.; Zhang, H. (2004). Studies on Screening for γ-aminobutyric acid producer and optimization of fermentation conditions. Chin. J. Amino Acids Biotic Res. 26(1), 40-43.
52. Lu, X.; Xie, C.; Gu, Z. (2008). Isolation of γ-aminobutyric acidproducing bacteria and optimization of fermentative medium. Biochem. Eng. J. 41, 48-52.
53. Lu, X.; Xie, C.; Gu, Z. (2009). Optimisation of fermentative parameters for GABA enrichment by Lactococcus lactis. Czech. J. Food Sci. 27(6), 433-442.
54. Maras, B.; Sweeney, G.; Barra, D.; Bossa, F.; John, R.A. (1992). The amino acid sequence of glutamate decarboxylase from Escherichia coli. Eur. J. Biochem. 204, 93-98.
55. Miura, D.; Ito, Y.; Mizukuchi, A.; Kise, M.; Aoto, H.; Yagasaki, K. (2006). Hypercholesterolemic action of pre-germinated brown rice in hepatoma-bearing rats. Life Sci. 79, 259-264.
56. Nikolaeva, Z. K.; Yu, V.V. (1972). Mechanism of action of yaminobutyrate-glutamate transaminase from pig kidney. Biokhimiya 37, 572-578.
57. 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.
58. 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.
59. 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. Jap. Soc. Food Sci. 47, 596-603.
60. Park, K.B.; Oh, S.H. (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.
61. Park, K.B.; Oh, S.H. (2007). 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.
62. Pimentel, M.C.B.; Melo, E.H.M.; Filho, J.L.L. (1996). DURAN N. Production of lipase free of citrinin by Penicillium citrinum. Mycopathologia 133, 119-121.
63. Plokhov, A.Y.; Gusyatiner, M.M.; Yampolskaya, T.A.; Kaluzhsky, V.E.; Sukhareva, B.S.; Schulga, A.A. (2000). Preparation of gammaaminobutyric acid using E. coli cells with high activity of glutamate decarboxylase. Appl. Biochem. Biotechnol. 88, 257-265.
64. Reed, L. J. (1950). The occurrence of c-aminobutyric acid in yeast extract; its isolation and identification. J. Biol. Chem. 183, 451-458.
65. Rizzello, C.G.; Cassone, A.; Cagno, R. DI.; Gobbetti, M. (2008). 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. 56, 6936-6943.
66. Saikusa, T.; Horino, T.; Mori Y. (1994). Accumulation of gaminobutyric acid (Gaba) in the rice germ during water soaking. Biosci. Biotech. Biochem. 58, 2291-2292.
67. Sanders, J. W.; Leenhouts, K.; Burghoorn, J.; Brands, J. R.; Venema, G.; Kok, J. (1998.) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol. Microbiol. 27, 299-310.
68. Sandmeier, E.; Hale, T.I.; Christen, P. (1994). Multiple evolutionary origin of pyridoxal 50-phosphate-dependent amino acid decarboxylase. Eur. J. Biochem. 221, 997-1002.
69. Sawai, Y.; Yamaguchi, Y.; Miyana, D.; Yoshitomi, H. (2001). Cycling treatment of anaerobic and aerobic incubation increases the content of gaminobutyric acid in tea shoots. Amino Acids 20, 331-334.
70. Schmit, J. C.; Brody, S. (1975). Neurospora crassa conidial germination: role of endogenous amino acid pools. J. Bacteriol. 124, 232-242.
71. Scott, E. M.; Jakoby, W. B. (1959). Soluble y-aminobutyric-glutamic transaminase from Pseudomonas fluorescens. J. Biol. Chem. 234, 932-936.
72. Servili, M.; Rizzello, C.G.; Taticchi, A.; Esposto, S.; Urbani, S.; Mazzacane, F.; Di Maio, I.; Selvaggini, R.; Gobbetti, M.; Di Cagno, R. (2011). Functional milk beverage fortified with phenolic compounds extracted from olive vegetation water, and fermented with functional lactic acid bacteria. Int. J. Food Microbiol. 147(1), 45-52.
73. Settanni, L.; Corsetti, A. (2008). Application of bacteriocins in vegetable food biopreservation. Int. J. Food Microbiol. 121, 123-138.
74. 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 gamma-aminobutyric acid. Food Sci. Biotechnol. 17, 940-946.
75. Shelp, B. J.; Bown, A. W.; Mclean, M. D. (1999). Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 4, 446-452.
76. Siragusa, S.; Angelis, M. De.; Cagno, R. Di.; Rizzello, C. G.; Coda, R.; Gobbetti, M. (2007). Synthesis of γ-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl. Environ. Microbiol. 7283-7290.
77. Skeie, S.; Lindberg, C.; Narvhus, J. (2001). Development of amino acids and organic acids in Norvegia, influence of milk treatment and adjunct Lactobacillus. Int. Dairy J. 11, 399-411.
78. Smith, D.K.; Kassam, T.; Singh, B.; Elliott, J.F. (1992). Escherichia coli has two homologousglutamate decarboxylase genes that map to distinct loci. J. Bacteriol. 174, 5820-5826.
79. Soo, I.M.C.; Lee, J.W.; Park, S.M.; Lee, M.Y.; Ji, G.E.; Park, M.S.; Heo, T.R. (2006). Improvement of γ-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 16(4), 562-568.
80. Steward, F.C.; Thompson, J. F.; Dent, C. E. (1949). γ-aminobutyric acid: a constituent of the potato tuber? Science 110, 439-440.
81. Su, Y.C.; Wang, J.J.; Lin, T.T.; Pan, T.M. (2003). Production of the secondary metabolites gamma-aminobutyric acid and monacolin K by Monascus. J. Ind. Microbiol. Biotechnol. 30, 41-46.
82. Sun, B.S.; Zhou, L.P.; Jia, X.Q.; Sung, C.K. (2008). Response surface modeling for g-aminobutyric acid production by Monascus pilosus GM100 under solid-state fermentation. Afr. J. Biotechnol. 7(24), 4544-4550.
83. Tsai, J.S.; Lin, Y.S.; Pan, B.S.; Chen, T.J. (2006). Antihypertensive peptides and gamma-aminobutyric acid from prozyme 6 facilitated lactic acid bacteria fermentation of soymilk. Process Biochem. 41, 1282-1288.
84. Tsushida, T.; Murai, T. (1987). Conversion of glutamic acid to gaminobutyric acid in tea leaves under anaerobic conditions. Agric. Biol. Chem. 51, 2865-2871.
85. Ueno, H. (2000). Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B: Enzym. 10, 67-79.
86. Ueno, Y.; Hayakawa, K.; Takahashi, S.; Oda, K. (1997). Purification and characterization of glutamate decarboxylase from Lactobacillus brevis IFO 12005. Biosci. Biotech. Biochem. 61, 1168-1171.
87. Voellmy, R.; Leisinger, T. (1976). Role of 4-aminobutyrate aminotransferase in the arginine metabolism of Pseudomonas aeruginosa. J. Bacteriol. 128(3), 722-729.
88. Wang, J.J.; Lee, C.L.; Pan, T.M. (2003). 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. 30, 669-676.
89. Wouters, J.T.M.; Ayad, E.H.; Hugenholtz, J.; Smit, G. (2002). Microbes from raw milk for fermented dairy products. Int. Dairy J. 12, 91-109.
90. Yang, S.Y.; Lu, F.X.; Lu, Z.X.; Bie, X.M.; Jiao, Y.; Sun, L.J.; Yu, B. (2008). Production of gamma-aminobutyric acid by Streptococcus salivarius subsp thermophilus Y2 under submerged fermentation. Amino Acids 34, 473-478.
91. Yokoyama, S.; Hiramatsu, J.; Hayakawa, K. (2002). Production of yaminobutyric acid from alcohol distillery lees by Lactobacilus brevis IFO-12005. J. Biosci. Bioeng. 93(1), 95-97.