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References

  1. Manyam BV, Katz L, Hare TA, Kaniefski K, Tremblay RD. 1981. Isoniazid-induced elevation of CSF GABA levels and effects on chorea in Huntington’s disease. Ann. Neurol. 10:35-37.
    Pubmed CrossRef
  2. Ueno H. 2000. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B Enzym. 10: 67-79.
    CrossRef
  3. Tsai JS, Lin YS, Pan BS, Chen TJ. 2006. Antihypertensive peptides and γ-aminobutyric acid from prozyme 6 facilitated lactic acid bacteria fermentation of soymilk. Process Biochem. 41: 1282-1288.
    CrossRef
  4. Wong CG, Bottiglieri T, Snead OC III. 2003. GABA, γhydroxybutyric acid, and neurological disease. Ann Neurol. 54: S3-S12.
    Pubmed CrossRef
  5. Kim JY, Lee MY, Ji GE, Lee YS, Hwang KT. 2009. Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int. J. Food Microbiol. 130: 12-16.
    Pubmed CrossRef
  6. Dhakal R, Bajpai VK, Baek KH. 2012. Production of GABA (γ-aminobutyric acid) by microorganisms: a review. Braz. J. Microbiol. 43: 1230-1241.
    Pubmed PMC CrossRef
  7. 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. Int. J. Food Sci. Technol. 45: 594-601.
    CrossRef
  8. Naidu AS, Bidlack WR, Clemens RA. 1999. Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutr. 39: 13-126.
    Pubmed CrossRef
  9. Di Cagno R, Mazzacane F, Rizzello CG, De Angelis M, Giuliani G, Meloni M, et al. 2010. Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl. Microbiol. Biotechnol. 86: 731-741.
    Pubmed CrossRef
  10. 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: 7283-7290.
    Pubmed PMC CrossRef
  11. 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
  12. Cho YR, Chang JY, Chang HC. 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.
    Pubmed
  13. Seo MJ, Nam YD, Lee SY, Park SL, Yi SH, Lim SI. 2013. Expression and characterization of a glutamate decarboxylase from Lactobacillus brevis 877G producing γ-aminobutyric acid. Biosci. Biotechnol. Biochem. 77: 853-856.
    Pubmed CrossRef
  14. Hiraga K, Ueno Y, Sukontasing S, Tanasupawat S, Oda K. 2008. Lactobacillus senmaizukei sp. nov., isolated from Japanese pickle. Int. J. Syst. Evol. Microbiol. 58: 1625-1629.
    Pubmed CrossRef
  15. Seo MJ, Lee JY, Nam YD, Lee SY, Park SL, Yi SH, et al. 2013. Production of γ-aminobutyric acid by Lactobacillus brevis 340G isolated from kimchi and its application to skim milk. Food Eng. Prog. 17: 418-423.
    CrossRef
  16. Kumar P, Satyanarayana T. 2007. Optimization of culture variables for improving glucoamylase production by alginateentrapped Thermomucor indicae-seudaticae using statistical methods. Bioresour. Technol. 98: 1252-1259.
    Pubmed CrossRef
  17. Sun Y, Li T, Yan J, Liu J. 2010. Technology optimization for polysaccharides (POP) extraction from the fruiting bodies of Pleurotus ostreatus by Box-Behnken statistical design. Carbohydr. Polym. 80: 242-247.
    CrossRef
  18. Zhong K, Wang Q. 2010. Optimization of ultrasonic extraction of polysaccharides from dried longan pulp using response surface methodology. Carbohydr. Polym. 80: 19-25.
    CrossRef
  19. Survase SA, Annapure US, Singhal RS. 2009. Statistical optimization for improved production of cyclosporine A in solid-state fermentation. J. Microbiol. Biotechnol. 19: 1385-1392.
    Pubmed CrossRef
  20. Binh TTT, Ju WT, Jung WJ, Park RD. 2014. Optimization of γ-amino butyric acid production in a newly isolated Lactobacillus brevis. Biotechnol. Lett. 36: 93-98.
    Pubmed CrossRef
  21. Kook MC, Seo MJ, Cheigh CI, Pyun YR, Cho SC, Park H. 2010. Enhanced production of gamma-aminobutyric acid using rice bran extracts by Lactobacillus sakei B2-16. J. Microbiol. Biotechnol. 20: 763-766.
    Pubmed
  22. Lim HS, Cha I, Lee H, Seo MJ. 2016. Optimization of γ-aminobutyric acid production by Enterococcus faecium JK29 isolated from a traditional fermented foods. Microbiol. Biotechnol. Lett. 44: 26-33.
    CrossRef
  23. Lu X, Xie C, Gu Z. 2009. Optimisation of fermentative parameters for GABA enrichment by Lactococcus lactis. Czech J. Food Sci. 27: 433-442.
  24. Tajabadi N, Ebrahimpour A, Baradaran A, Rahim RA, Mahyudin NA, Manap MYA, et al. 2015. Optimization of γ-aminobutyric acid production by Lactobacillus plantarum Taj-Apis362 from honeybees. Molecules 20: 6654-6669.
    Pubmed CrossRef
  25. Holdiness MR. 1983. Chromatographic analysis of glutamic acid decarboxylase in biological samples. J. Chromatogr. 277: 1-24.
    CrossRef
  26. Zhang G, Bown AW. 1997. The rapid determination of γ-aminobutyric acid. Phytochemistry 44: 1007-1009.
    CrossRef
  27. Kim JK, Park SY, Lim SH, Yeo Y, Cho HS, Ha SH. 2013. Comparative metabolic profiling of pigmented rice (Oryza sativa L.) cultivars reveals primary metabolites are correlated with secondary metabolites. J. Cereal Sci. 57: 14-20.
    CrossRef
  28. Wang JJ, Lee CJ, Pan TM. 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.
    Pubmed CrossRef
  29. Huang G, Mao J, Ji Z, Fu J, Zou H. 2013. Optimization of culture medium formulation for γ-aminobutyric acid-producing Lactobacillus plantarum MJ0301. Food Sci. (China) 34: 165-170.
  30. Park KB, Kim YH, Oh SH. 2009. Optimization of γ-aminobutyric acid production by fermenting with Lactobacillus sp. OPK. FASEB J. 23: Suppl. 719.7.
  31. Komatsuzaki N, Shima J, Kawamotoa S, Momosed H, Kimurab T. 2005. Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22: 497-504.
    CrossRef
  32. Li H, Qiu T, Huang G, Cao Y. 2010. Production of gammaaminobutyric acid by Lactobacillus brevis NCL912 using fedbatch fermentation. Microb. Cell Fact. 9: 85.
    Pubmed PMC CrossRef
  33. Yang SY, Lü 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.
    Pubmed CrossRef
  34. Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 3525-3535.
    Pubmed PMC
  35. 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.
    Pubmed CrossRef
  36. Yang H, Xing R, Hu L, Liu S, Li P. 2016. 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
  37. Rastogi NK, Rashmi KR. 1999. Optimisation of enzymatic liquefaction of mango pulp by response surface methodology. Eur. Food Res. Technol. 209: 57-62.
    CrossRef
  38. Yoon CH, Bok HS, Choi DK, Row KH. 2012. Optimization condition of astaxanthin extract from shrimp waste using response surface methodology. Korean Chem. Eng. Res. 50:545-550.
    CrossRef
  39. 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.
    Pubmed CrossRef
  40. Choi SI, Lee JW, Park SM, Lee MY, Ji GE, Park MS, Heo TR. 2006. Improvement of γ-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 16: 562-568.
  41. Kantachote D, Nunkaew T, Ratanaburee A, Klongdee N. 2016. Production of a meat seasoning powder enriched with γ-aminobutyric acid (GABA) from mature coconut water using Pediococcus pentosaceus HN8. J. Food Process. Preserv. 40: 733-742.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(3): 450-459

Published online March 28, 2017 https://doi.org/10.4014/jmb.1610.10008

Copyright © The Korean Society for Microbiology and Biotechnology.

Enhanced Production of Gamma-Aminobutyric Acid by Optimizing Culture Conditions of Lactobacillus brevis HYE1 Isolated from Kimchi, a Korean Fermented Food

Hee Seon Lim 1, In-Tae Cha 2, Seong Woon Roh 3, Hae-Hun Shin 4 and Myung-Ji Seo 1, 2*

1Department of Life Sciences, Graduate School of Incheon National University, Incheon 22012, Republic of Korea, 2Division of Bioengineering, Incheon National University, Incheon 22012, Republic of Korea, 3Biological Disaster Analysis Group, Korea Basic Science Institute, Daejeon 34133, Republic of Korea, 4Division of Foodservice Industry, Baekseok Culture University, Chungnam 31065, Republic of Korea

Received: October 6, 2016; Accepted: November 15, 2016

Abstract

This study evaluated the effects of culture conditions, including carbon and nitrogen sources,
L-monosodium glutamate (MSG), and initial pH, on gamma-aminobutyric acid (GABA)
production by Lactobacillus brevis HYE1 isolated from kimchi, a Korean traditional fermented
food. L. brevis HYE1 was screened by the production analysis of GABA and genetic analysis of
the glutamate decarboxylase gene, resulting in 14.64 mM GABA after 48 h of cultivation in
MRS medium containing 1% (w/v) MSG. In order to increase GABA production by L. brevis
HYE1, the effects of carbon and nitrogen sources on GABA production were preliminarily
investigated via one-factor-at-a-time optimization strategy. As the results, 2% maltose and 3%
tryptone were determined to produce 17.93 mM GABA in modified MRS medium with 1%
(w/v) MSG. In addition, the optimal MSG concentration and initial pH were determined to be
1% and 5.0, respectively, resulting in production of 18.97 mM GABA. Thereafter, response
surface methodology (RSM) was applied to determine the optimal conditions of the above four
factors. The results indicate that pH was the most significant factor for GABA production. The
optimal culture conditions for maximum GABA production were also determined to be 2.14%
(w/v) maltose, 4.01% (w/v) tryptone, 2.38% (w/v) MSG, and an initial pH of 4.74. In these
conditions, GABA production by L. brevis HYE1 was predicted to be 21.44 mM using the RSM
model. The experiment was performed under these optimized conditions, resulting in GABA
production of 18.76 mM. These results show that the predicted and experimental values of
GABA production are in good agreement.

Keywords: Gamma-aminobutyric acid, Lactobacillus brevis, optimization, response surface methodology, fermented food

References

  1. Manyam BV, Katz L, Hare TA, Kaniefski K, Tremblay RD. 1981. Isoniazid-induced elevation of CSF GABA levels and effects on chorea in Huntington’s disease. Ann. Neurol. 10:35-37.
    Pubmed CrossRef
  2. Ueno H. 2000. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B Enzym. 10: 67-79.
    CrossRef
  3. Tsai JS, Lin YS, Pan BS, Chen TJ. 2006. Antihypertensive peptides and γ-aminobutyric acid from prozyme 6 facilitated lactic acid bacteria fermentation of soymilk. Process Biochem. 41: 1282-1288.
    CrossRef
  4. Wong CG, Bottiglieri T, Snead OC III. 2003. GABA, γhydroxybutyric acid, and neurological disease. Ann Neurol. 54: S3-S12.
    Pubmed CrossRef
  5. Kim JY, Lee MY, Ji GE, Lee YS, Hwang KT. 2009. Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. Int. J. Food Microbiol. 130: 12-16.
    Pubmed CrossRef
  6. Dhakal R, Bajpai VK, Baek KH. 2012. Production of GABA (γ-aminobutyric acid) by microorganisms: a review. Braz. J. Microbiol. 43: 1230-1241.
    Pubmed KoreaMed CrossRef
  7. 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. Int. J. Food Sci. Technol. 45: 594-601.
    CrossRef
  8. Naidu AS, Bidlack WR, Clemens RA. 1999. Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutr. 39: 13-126.
    Pubmed CrossRef
  9. Di Cagno R, Mazzacane F, Rizzello CG, De Angelis M, Giuliani G, Meloni M, et al. 2010. Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl. Microbiol. Biotechnol. 86: 731-741.
    Pubmed CrossRef
  10. 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: 7283-7290.
    Pubmed KoreaMed CrossRef
  11. 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
  12. Cho YR, Chang JY, Chang HC. 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.
    Pubmed
  13. Seo MJ, Nam YD, Lee SY, Park SL, Yi SH, Lim SI. 2013. Expression and characterization of a glutamate decarboxylase from Lactobacillus brevis 877G producing γ-aminobutyric acid. Biosci. Biotechnol. Biochem. 77: 853-856.
    Pubmed CrossRef
  14. Hiraga K, Ueno Y, Sukontasing S, Tanasupawat S, Oda K. 2008. Lactobacillus senmaizukei sp. nov., isolated from Japanese pickle. Int. J. Syst. Evol. Microbiol. 58: 1625-1629.
    Pubmed CrossRef
  15. Seo MJ, Lee JY, Nam YD, Lee SY, Park SL, Yi SH, et al. 2013. Production of γ-aminobutyric acid by Lactobacillus brevis 340G isolated from kimchi and its application to skim milk. Food Eng. Prog. 17: 418-423.
    CrossRef
  16. Kumar P, Satyanarayana T. 2007. Optimization of culture variables for improving glucoamylase production by alginateentrapped Thermomucor indicae-seudaticae using statistical methods. Bioresour. Technol. 98: 1252-1259.
    Pubmed CrossRef
  17. Sun Y, Li T, Yan J, Liu J. 2010. Technology optimization for polysaccharides (POP) extraction from the fruiting bodies of Pleurotus ostreatus by Box-Behnken statistical design. Carbohydr. Polym. 80: 242-247.
    CrossRef
  18. Zhong K, Wang Q. 2010. Optimization of ultrasonic extraction of polysaccharides from dried longan pulp using response surface methodology. Carbohydr. Polym. 80: 19-25.
    CrossRef
  19. Survase SA, Annapure US, Singhal RS. 2009. Statistical optimization for improved production of cyclosporine A in solid-state fermentation. J. Microbiol. Biotechnol. 19: 1385-1392.
    Pubmed CrossRef
  20. Binh TTT, Ju WT, Jung WJ, Park RD. 2014. Optimization of γ-amino butyric acid production in a newly isolated Lactobacillus brevis. Biotechnol. Lett. 36: 93-98.
    Pubmed CrossRef
  21. Kook MC, Seo MJ, Cheigh CI, Pyun YR, Cho SC, Park H. 2010. Enhanced production of gamma-aminobutyric acid using rice bran extracts by Lactobacillus sakei B2-16. J. Microbiol. Biotechnol. 20: 763-766.
    Pubmed
  22. Lim HS, Cha I, Lee H, Seo MJ. 2016. Optimization of γ-aminobutyric acid production by Enterococcus faecium JK29 isolated from a traditional fermented foods. Microbiol. Biotechnol. Lett. 44: 26-33.
    CrossRef
  23. Lu X, Xie C, Gu Z. 2009. Optimisation of fermentative parameters for GABA enrichment by Lactococcus lactis. Czech J. Food Sci. 27: 433-442.
  24. Tajabadi N, Ebrahimpour A, Baradaran A, Rahim RA, Mahyudin NA, Manap MYA, et al. 2015. Optimization of γ-aminobutyric acid production by Lactobacillus plantarum Taj-Apis362 from honeybees. Molecules 20: 6654-6669.
    Pubmed CrossRef
  25. Holdiness MR. 1983. Chromatographic analysis of glutamic acid decarboxylase in biological samples. J. Chromatogr. 277: 1-24.
    CrossRef
  26. Zhang G, Bown AW. 1997. The rapid determination of γ-aminobutyric acid. Phytochemistry 44: 1007-1009.
    CrossRef
  27. Kim JK, Park SY, Lim SH, Yeo Y, Cho HS, Ha SH. 2013. Comparative metabolic profiling of pigmented rice (Oryza sativa L.) cultivars reveals primary metabolites are correlated with secondary metabolites. J. Cereal Sci. 57: 14-20.
    CrossRef
  28. Wang JJ, Lee CJ, Pan TM. 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.
    Pubmed CrossRef
  29. Huang G, Mao J, Ji Z, Fu J, Zou H. 2013. Optimization of culture medium formulation for γ-aminobutyric acid-producing Lactobacillus plantarum MJ0301. Food Sci. (China) 34: 165-170.
  30. Park KB, Kim YH, Oh SH. 2009. Optimization of γ-aminobutyric acid production by fermenting with Lactobacillus sp. OPK. FASEB J. 23: Suppl. 719.7.
  31. Komatsuzaki N, Shima J, Kawamotoa S, Momosed H, Kimurab T. 2005. Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22: 497-504.
    CrossRef
  32. Li H, Qiu T, Huang G, Cao Y. 2010. Production of gammaaminobutyric acid by Lactobacillus brevis NCL912 using fedbatch fermentation. Microb. Cell Fact. 9: 85.
    Pubmed KoreaMed CrossRef
  33. Yang SY, Lü 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.
    Pubmed CrossRef
  34. Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 3525-3535.
    Pubmed KoreaMed
  35. 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.
    Pubmed CrossRef
  36. Yang H, Xing R, Hu L, Liu S, Li P. 2016. 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
  37. Rastogi NK, Rashmi KR. 1999. Optimisation of enzymatic liquefaction of mango pulp by response surface methodology. Eur. Food Res. Technol. 209: 57-62.
    CrossRef
  38. Yoon CH, Bok HS, Choi DK, Row KH. 2012. Optimization condition of astaxanthin extract from shrimp waste using response surface methodology. Korean Chem. Eng. Res. 50:545-550.
    CrossRef
  39. 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.
    Pubmed CrossRef
  40. Choi SI, Lee JW, Park SM, Lee MY, Ji GE, Park MS, Heo TR. 2006. Improvement of γ-aminobutyric acid (GABA) production using cell entrapment of Lactobacillus brevis GABA 057. J. Microbiol. Biotechnol. 16: 562-568.
  41. Kantachote D, Nunkaew T, Ratanaburee A, Klongdee N. 2016. Production of a meat seasoning powder enriched with γ-aminobutyric acid (GABA) from mature coconut water using Pediococcus pentosaceus HN8. J. Food Process. Preserv. 40: 733-742.
    CrossRef