DOI QR코드

DOI QR Code

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

  • Lim, Hee Seon (Department of Life Sciences, Graduate School of Incheon National University) ;
  • Cha, In-Tae (Division of Bioengineering, Incheon National University) ;
  • Roh, Seong Woon (Biological Disaster Analysis Group, Korea Basic Science Institute) ;
  • Shin, Hae-Hun (Division of Foodservice Industry, Baekseok Culture University) ;
  • Seo, Myung-Ji (Department of Life Sciences, Graduate School of Incheon National University)
  • Received : 2016.10.06
  • Accepted : 2016.11.15
  • Published : 2017.03.28

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

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. https://doi.org/10.1002/ana.410100107
  2. Ueno H. 2000. Enzymatic and structural aspects on glutamate decarboxylase. J. Mol. Catal. B Enzym. 10: 67-79. https://doi.org/10.1016/S1381-1177(00)00114-4
  3. 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. https://doi.org/10.1016/j.procbio.2005.12.026
  4. Wong CG, Bottiglieri T, Snead OC III. 2003. GABA, ${\gamma}$-hydroxybutyric acid, and neurological disease. Ann Neurol. 54: S3-S12.
  5. 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. https://doi.org/10.1016/j.ijfoodmicro.2008.12.028
  6. Dhakal R, Bajpai VK, Baek KH. 2012. Production of GABA (${\gamma}$-aminobutyric acid) by microorganisms: a review. Braz. J. Microbiol. 43: 1230-1241. https://doi.org/10.1590/S1517-83822012000400001
  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. https://doi.org/10.1111/j.1365-2621.2010.02172.x
  8. Naidu AS, Bidlack WR, Clemens RA. 1999. Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutr. 39: 13-126. https://doi.org/10.1080/10408699991279187
  9. Di Cagno R, Mazzacane F, Rizzello CG, De Angelis M, Giuliani G, Meloni M, et al. 2010. Synthesis of ${\gamma}$-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: functional grape must beverage and dermatological applications. Appl. Microbiol. Biotechnol. 86: 731-741. https://doi.org/10.1007/s00253-009-2370-4
  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. https://doi.org/10.1128/AEM.01064-07
  11. 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. https://doi.org/10.3168/jds.S0022-0302(98)75714-5
  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.
  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 ${\gamma}$-aminobutyric acid. Biosci. Biotechnol. Biochem. 77: 853-856. https://doi.org/10.1271/bbb.120785
  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. https://doi.org/10.1099/ijs.0.65677-0
  15. Seo MJ, Lee JY, Nam YD, Lee SY, Park SL, Yi SH, et al. 2013. Production of ${\gamma}$-aminobutyric acid by Lactobacillus brevis 340G isolated from kimchi and its application to skim milk. Food Eng. Prog. 17: 418-423. https://doi.org/10.13050/foodengprog.2013.17.4.418
  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. https://doi.org/10.1016/j.biortech.2006.05.019
  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. https://doi.org/10.1016/j.carbpol.2009.11.018
  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. https://doi.org/10.1016/j.carbpol.2009.10.066
  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.
  20. Binh TTT, Ju WT, Jung WJ, Park RD. 2014. Optimization of ${\gamma}$-amino butyric acid production in a newly isolated Lactobacillus brevis. Biotechnol. Lett. 36: 93-98. https://doi.org/10.1007/s10529-013-1326-z
  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.
  22. Lim HS, Cha I, Lee H, Seo MJ. 2016. Optimization of ${\gamma}$-aminobutyric acid production by Enterococcus faecium JK29 isolated from a traditional fermented foods. Microbiol. Biotechnol. Lett. 44: 26-33. https://doi.org/10.4014/mbl.1512.12004
  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 ${\gamma}$-aminobutyric acid production by Lactobacillus plantarum Taj-Apis362 from honeybees. Molecules 20: 6654-6669. https://doi.org/10.3390/molecules20046654
  25. Holdiness MR. 1983. Chromatographic analysis of glutamic acid decarboxylase in biological samples. J. Chromatogr. 277: 1-24. https://doi.org/10.1016/S0378-4347(00)84819-7
  26. Zhang G, Bown AW. 1997. The rapid determination of ${\gamma}$-aminobutyric acid. Phytochemistry 44: 1007-1009. https://doi.org/10.1016/S0031-9422(96)00626-7
  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. https://doi.org/10.1016/j.jcs.2012.09.012
  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. https://doi.org/10.1007/s10295-003-0097-2
  29. Huang G, Mao J, Ji Z, Fu J, Zou H. 2013. Optimization of culture medium formulation for ${\gamma}$-aminobutyric acid-producing Lactobacillus plantarum MJ0301. Food Sci. (China) 34: 165-170.
  30. Park KB, Kim YH, Oh SH. 2009. Optimization of ${\gamma}$-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 ${\gamma}$-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22: 497-504. https://doi.org/10.1016/j.fm.2005.01.002
  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. https://doi.org/10.1186/1475-2859-9-85
  33. 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. https://doi.org/10.1007/s00726-007-0544-x
  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.
  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. https://doi.org/10.1046/j.1365-2958.1998.00676.x
  36. Yang H, Xing R, Hu L, Liu S, Li P. 2016. Accumulation of ${\gamma}$-aminobutyric acid by Enterococcus avium 9184 in scallop solution in a two-stage fermentation strategy. Microb. Biotechnol. 9: 478-485. https://doi.org/10.1111/1751-7915.12301
  37. Rastogi NK, Rashmi KR. 1999. Optimisation of enzymatic liquefaction of mango pulp by response surface methodology. Eur. Food Res. Technol. 209: 57-62. https://doi.org/10.1007/s002170050457
  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. https://doi.org/10.9713/kcer.2012.50.3.545
  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. https://doi.org/10.1007/s00726-009-0355-3
  40. 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.
  41. Kantachote D, Nunkaew T, Ratanaburee A, Klongdee N. 2016. Production of a meat seasoning powder enriched with ${\gamma}$-aminobutyric acid (GABA) from mature coconut water using Pediococcus pentosaceus HN8. J. Food Process. Preserv. 40: 733-742. https://doi.org/10.1111/jfpp.12654

Cited by

  1. Identification of 2-hydroxyisocaproic acid production in lactic acid bacteria and evaluation of microbial dynamics during kimchi ripening vol.7, pp.None, 2017, https://doi.org/10.1038/s41598-017-10948-0
  2. Expression and characterization of glutamate decarboxylase from Lactobacillus brevis HYE1 isolated from kimchi vol.34, pp.3, 2017, https://doi.org/10.1007/s11274-018-2427-6
  3. Substrate sustained release-based high efficacy biosynthesis of GABA by Lactobacillus brevis NCL912 vol.17, pp.None, 2017, https://doi.org/10.1186/s12934-018-0919-6
  4. Characteristics of Potential Gamma-Aminobutyric Acid-Producing Bacteria Isolated from Korean and Vietnamese Fermented Fish Products vol.29, pp.2, 2017, https://doi.org/10.4014/jmb.1811.09072
  5. Genomic insights into a robust gamma-aminobutyric acid-producer Lactobacillus brevis CD0817 vol.9, pp.None, 2019, https://doi.org/10.1186/s13568-019-0799-0
  6. Low-Cost Cultivation and Sporulation of Alkaliphilic Bacillus sp. Strain AK13 for Self-Healing Concrete vol.29, pp.12, 2017, https://doi.org/10.4014/jmb.1908.08034
  7. Isolation of Lactobacillus plantarum subsp. plantarum Producing C30 Carotenoid 4,4'-Diaponeurosporene and the Assessment of Its Antioxidant Activity vol.29, pp.12, 2019, https://doi.org/10.4014/jmb.1909.09007
  8. Development of Kinetic Models and Their Applications to Describe the Resistance of Listeria monocytogenes in Napa Cabbage Kimchi to Fermentation Conditions vol.26, pp.1, 2017, https://doi.org/10.3136/fstr.26.53
  9. Beneficial effect of GABA-rich fermented milk on insomnia involving regulation of gut microbiota vol.233, pp.None, 2017, https://doi.org/10.1016/j.micres.2020.126409
  10. The growth and potential of gamma-aminobutyric acid (GABA) by lactic acid bacteria isolated from fish fermented food from Maluku, Indonesia vol.1524, pp.None, 2020, https://doi.org/10.1088/1742-6596/1524/1/012133
  11. Beans germination as a potential tool for GABA-enriched tofu production vol.57, pp.11, 2017, https://doi.org/10.1007/s13197-020-04423-4
  12. Comparative Peptidomic and Metatranscriptomic Analyses Reveal Improved Gamma-Amino Butyric Acid Production Machinery in Levilactobacillus brevis Strain NPS-QW 145 Cocultured with Streptococcus thermop vol.87, pp.1, 2017, https://doi.org/10.1128/aem.01985-20
  13. Genome analysis and optimization of γ-aminobutyric acid (GABA) production by lactic acid bacteria from plant materials vol.67, pp.4, 2021, https://doi.org/10.2323/jgam.2020.10.002
  14. Environmental Conditions Affecting GABA Production in Lactococcus lactis NCDO 2118 vol.9, pp.1, 2017, https://doi.org/10.3390/microorganisms9010122
  15. Development of Puffed Grain Products Containing Synbiotic Materials Using Electrostatic Spray vol.50, pp.2, 2017, https://doi.org/10.3746/jkfn.2021.50.2.185
  16. Probiotics, Prebiotics and Postbiotics on Mitigation of Depression Symptoms: Modulation of the Brain-Gut-Microbiome Axis vol.11, pp.7, 2017, https://doi.org/10.3390/biom11071000
  17. Glutamate and depression: Reflecting a deepening knowledge of the gut and brain effects of a ubiquitous molecule vol.11, pp.7, 2017, https://doi.org/10.5498/wjp.v11.i7.297
  18. Lactic Acid Fermented Green Tea with Levilactobacillus brevis Capable of Producing γ-Aminobutyric Acid vol.7, pp.3, 2021, https://doi.org/10.3390/fermentation7030110
  19. Some Important Metabolites Produced by Lactic Acid Bacteria Originated from Kimchi vol.10, pp.9, 2017, https://doi.org/10.3390/foods10092148
  20. GABA enhancement by simple carbohydrates in yoghurt fermented using novel, self-cloned Lactobacillus plantarum Taj-Apis362 and metabolomics profiling vol.11, pp.1, 2017, https://doi.org/10.1038/s41598-021-88436-9