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References

  1. Manyam BV, Catz L, Hare TA, Kaniefski K, Tremblay RD. 1981. Isoniazid-induced elevation of cerebrospinal fluid (CSF) GABA levels and effects on chorea in Huntington’s disease. Ann. Neurol. 10: 35-37.
    Pubmed CrossRef
  2. Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M. 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.
    Pubmed CrossRef
  3. Jakobs C, Jaeken J, Gibson KM. 1993. Inherited disorders of GABA metabolism. J. Inherit. Metab. Dis. 16: 704-715.
    Pubmed CrossRef
  4. Wong CG, Bottiglieri T, Snead OC 3rd. 2003. GABA, γaminobutyric acid, and neurological disease. Ann. Neurol. 54: S3-S12.
    Pubmed CrossRef
  5. Park KB, Oh SH. 2007. 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.
    Pubmed CrossRef
  6. Li H, Cao Y. 2010. Lactic acid bacteria cell factories for gamma-aminobutyric acid. Amino acids 39: 1107-1116.
    Pubmed CrossRef
  7. 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 γ-aminobutyric acid. Biosci. Biotechnol. Biochem. 72: 3265-3272.
    Pubmed CrossRef
  8. Leory F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78.
    CrossRef
  9. Ueno H. 2000. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B Enzym. 10: 67-79.
    CrossRef
  10. Park JY, Jeong SJ, Kim JH. 2014. Characterization of a glutamate decarboxylase (GAD) gene from Lactobacillus zymae. Biotechnol. Lett. 36: 1791-1799.
    Pubmed CrossRef
  11. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
    Pubmed PMC CrossRef
  12. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  13. Tamura T, Noda M, Ozaki M, Maruyama M, Matoba Y, Kumagai T. 2010. Establishment of an efficient fermentation system of gamma-aminobutyric acid by a lactic acid bacterium, Enterococcus avium G-15, isolated from carrot leaves. Biol. Pharm. Bull. 33: 1673-1679.
    Pubmed CrossRef
  14. Hiraga K, Ueno Y, Oda K. 2008. Glutamate decarboxylase from Lactobacillus brevis: activation by ammonium sulfate. Biosci. Biotechnol. Biochem. 72: 1299-1306.
    Pubmed CrossRef
  15. Nomura M, Kimoto H, Someya Y, Furukawa S, Suzuki I. 1998. Production of γ-aminobutyric acid by cheese starters during cheese ripening. J. Dairy Sci. 81: 1486-1491.
    CrossRef
  16. Yokoyama S, Hiramatsu J, Hayakawa K. 2002. Production of γ-aminobutyric acid from alcohol distillery lees by Lactobacillus brevis IFO-12005. J. Biosci. Bioeng. 93: 95-97.
    CrossRef
  17. Siragusa S, Angelis MD, Cagno RD, 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.
    Pubmed PMC CrossRef
  18. Sa HD, Park JY, Jeong SJ, Lee KW, Kim JH. 2015. Characterization of glutamate decarboxylase (GAD) from Lactobacillus sakei A156 isolated from Jeot-gal. J. Microbiol. Biotechnol. 25: 696-703.
    Pubmed CrossRef
  19. 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.
    Pubmed
  20. Lim HS, Cha IT, Lee HJ, Seo MJ. 2016. Optimization of γ-aminobutyric acid production by Enterococcus faecium JK29 isolated from traditional fermented foods. Microbiol. Biotechnol. Lett. 44: 26-33.
    CrossRef
  21. Murzin AG. 1996. Structural classification of proteins: new super families. Curr. Opin. Struct. Biol. 6: 386-394.
    CrossRef
  22. Fonda ML. 1985. L-Glutamate decarboxylase from bacteria. Methods Enzymol. 113: 11-16.
    CrossRef
  23. Fan E, Huang J, Hu S, Mei L, Yu K. 2012. Cloning, sequencing and expression of a glutamate decarboxylase gene from the GABA-producing strain Lactobacillus brevis CGMCC1306. Ann. Microbiol. 62: 689-698.
    CrossRef
  24. Komatsuzaki N, Nakamura T, Kimura T, Shima J. 2008. Characterization of glutamate decarboxylase from a high γ-aminobutyric acid (GABA)-producer, Lactobacillus paracasei. Biosci. Biotechnol. Biochem. 72: 278-285.
    Pubmed CrossRef
  25. Lin Q, Yang S, Lu F, Lu Z, Bie X, Jiao Y, Zou X. 2009. Cloning and expression of glutamate decarboxylase gene from Streptococcus thermophiles Y2. J. Gen. Appl. Microbiol. 55: 305-310.
    Pubmed CrossRef
  26. Yang H, Xing R, Hu L, Liu S, Li P. 2015. Accumulation of γ-aminobutyric acid by Enterococcus avium 9184 in scallop solution in a two-stage fermentation strategy. Microb. Biotechnol. 9: 478-485.
    Pubmed PMC CrossRef
  27. Nomura M, Nakajima I, Fujita Y, Kobayashi M, Kimoto H, Suzuki I, Aso H. 1999. Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145: 1375-1380.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(7): 1216-1222

Published online July 28, 2017 https://doi.org/10.4014/jmb.1701.01058

Copyright © The Korean Society for Microbiology and Biotechnology.

Characterization of a Glutamate Decarboxylase (GAD) from Enterococcus avium M5 Isolated from Jeotgal, a Korean Fermented Seafood

Kang Wook Lee 1, Jae Min Shim 1, Zhuang Yao 1, Jeong A Kim 1, Hyun-Jin Kim 1, 2 and Jeong Hwan Kim 1, 2*

1Division of Applied Life Science (BK21 Plus), Graduate School,, 2Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Republic of Korea

Received: January 23, 2017; Accepted: April 23, 2017

Abstract

To develop starters for the production of functional foods or materials, lactic acid bacteria
producing γ-aminobutyric acid (GABA) were screened from jeotgals, Korean fermented
seafoods. One isolate producing a high amount of GABA from monosodium L-glutamate
(MSG) was identified as Enterococcus avium by 16S rRNA gene sequencing. E. avium M5
produced 18.47 ± 1.26 mg/ml GABA when incubated for 48 h at 37oC in MRS broth with MSG
(3% (w/v)). A gadB gene encoding glutamate decarboxylase (GAD) was cloned and
overexpressed in E. coli BL21 (DE3) using the pET26b (+) expression vector. Recombinant GAD
was purified through a Ni-NTA column and the size was estimated to be 53 kDa by SDSPAGE.
Maximum GAD activity was observed at pH 4.5 and 55oC and the activity was
dependent on pyridoxal 5’-phosphate. The Km and Vmax values of GAD were 3.26 ± 0.21 mM
and 0.0120 ± 0.0001 mM/min, respectively, when MSG was used as a substrate. Enterococcus
avium M5 secretes a lot of GABA when grown on MRS with MSG, and the strain is useful for
the production of fermented foods containing a high amount of GABA.

Keywords: Gamma-aminobutyric acid, glutamate decarboxylase, gad gene cloning, Enterococcus avium, jeotgal

References

  1. Manyam BV, Catz L, Hare TA, Kaniefski K, Tremblay RD. 1981. Isoniazid-induced elevation of cerebrospinal fluid (CSF) GABA levels and effects on chorea in Huntington’s disease. Ann. Neurol. 10: 35-37.
    Pubmed CrossRef
  2. Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M. 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.
    Pubmed CrossRef
  3. Jakobs C, Jaeken J, Gibson KM. 1993. Inherited disorders of GABA metabolism. J. Inherit. Metab. Dis. 16: 704-715.
    Pubmed CrossRef
  4. Wong CG, Bottiglieri T, Snead OC 3rd. 2003. GABA, γaminobutyric acid, and neurological disease. Ann. Neurol. 54: S3-S12.
    Pubmed CrossRef
  5. Park KB, Oh SH. 2007. 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.
    Pubmed CrossRef
  6. Li H, Cao Y. 2010. Lactic acid bacteria cell factories for gamma-aminobutyric acid. Amino acids 39: 1107-1116.
    Pubmed CrossRef
  7. 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 γ-aminobutyric acid. Biosci. Biotechnol. Biochem. 72: 3265-3272.
    Pubmed CrossRef
  8. Leory F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78.
    CrossRef
  9. Ueno H. 2000. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B Enzym. 10: 67-79.
    CrossRef
  10. Park JY, Jeong SJ, Kim JH. 2014. Characterization of a glutamate decarboxylase (GAD) gene from Lactobacillus zymae. Biotechnol. Lett. 36: 1791-1799.
    Pubmed CrossRef
  11. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
    Pubmed KoreaMed CrossRef
  12. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  13. Tamura T, Noda M, Ozaki M, Maruyama M, Matoba Y, Kumagai T. 2010. Establishment of an efficient fermentation system of gamma-aminobutyric acid by a lactic acid bacterium, Enterococcus avium G-15, isolated from carrot leaves. Biol. Pharm. Bull. 33: 1673-1679.
    Pubmed CrossRef
  14. Hiraga K, Ueno Y, Oda K. 2008. Glutamate decarboxylase from Lactobacillus brevis: activation by ammonium sulfate. Biosci. Biotechnol. Biochem. 72: 1299-1306.
    Pubmed CrossRef
  15. Nomura M, Kimoto H, Someya Y, Furukawa S, Suzuki I. 1998. Production of γ-aminobutyric acid by cheese starters during cheese ripening. J. Dairy Sci. 81: 1486-1491.
    CrossRef
  16. Yokoyama S, Hiramatsu J, Hayakawa K. 2002. Production of γ-aminobutyric acid from alcohol distillery lees by Lactobacillus brevis IFO-12005. J. Biosci. Bioeng. 93: 95-97.
    CrossRef
  17. Siragusa S, Angelis MD, Cagno RD, 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.
    Pubmed KoreaMed CrossRef
  18. Sa HD, Park JY, Jeong SJ, Lee KW, Kim JH. 2015. Characterization of glutamate decarboxylase (GAD) from Lactobacillus sakei A156 isolated from Jeot-gal. J. Microbiol. Biotechnol. 25: 696-703.
    Pubmed CrossRef
  19. 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.
    Pubmed
  20. Lim HS, Cha IT, Lee HJ, Seo MJ. 2016. Optimization of γ-aminobutyric acid production by Enterococcus faecium JK29 isolated from traditional fermented foods. Microbiol. Biotechnol. Lett. 44: 26-33.
    CrossRef
  21. Murzin AG. 1996. Structural classification of proteins: new super families. Curr. Opin. Struct. Biol. 6: 386-394.
    CrossRef
  22. Fonda ML. 1985. L-Glutamate decarboxylase from bacteria. Methods Enzymol. 113: 11-16.
    CrossRef
  23. Fan E, Huang J, Hu S, Mei L, Yu K. 2012. Cloning, sequencing and expression of a glutamate decarboxylase gene from the GABA-producing strain Lactobacillus brevis CGMCC1306. Ann. Microbiol. 62: 689-698.
    CrossRef
  24. Komatsuzaki N, Nakamura T, Kimura T, Shima J. 2008. Characterization of glutamate decarboxylase from a high γ-aminobutyric acid (GABA)-producer, Lactobacillus paracasei. Biosci. Biotechnol. Biochem. 72: 278-285.
    Pubmed CrossRef
  25. Lin Q, Yang S, Lu F, Lu Z, Bie X, Jiao Y, Zou X. 2009. Cloning and expression of glutamate decarboxylase gene from Streptococcus thermophiles Y2. J. Gen. Appl. Microbiol. 55: 305-310.
    Pubmed CrossRef
  26. Yang H, Xing R, Hu L, Liu S, Li P. 2015. Accumulation of γ-aminobutyric acid by Enterococcus avium 9184 in scallop solution in a two-stage fermentation strategy. Microb. Biotechnol. 9: 478-485.
    Pubmed KoreaMed CrossRef
  27. Nomura M, Nakajima I, Fujita Y, Kobayashi M, Kimoto H, Suzuki I, Aso H. 1999. Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145: 1375-1380.
    Pubmed CrossRef