Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2019 ; Vol.29-2: 209~221

AuthorThi Thu-Thao Vo, Jong-Hyun Park
Place of dutyGachon University, Seongnam, Republic of Korea
TitleCharacteristics of Potential Gamma-Aminobutyric Acid-Producing Bacteria Isolated from Korean and Vietnamese Fermented Fish Products
PublicationInfo J. Microbiol. Biotechnol.2019 ; Vol.29-2
AbstractGamma-aminobutyric acid (GABA) is a neurotransmitter that exerts several physiological functions and positive effects on human health. The aim of this study was to isolate and characterize the strains that had GABA-producing abilities from various fermented fish products. A total of 91 acid-producing strains were isolated from 41 samples of fermented fish products, and 27 strains showing GABA-producing abilities were identified by the 16S rDNA sequences. Among the strains, 31% strains tolerated at high-salt environment of 10–20% throughout the fermentation of fish sauces. The 27 isolates that produced GABA at various concentrations did so in the range of 5 to 454 mM. These GABA-producing isolates were identified as lactic acid bacteria of 14 strains, which included twelve Lactococcus lactis, one Enterococcus faecium, and one Lactococcus pentosus; eight Bacillus cereus group, which included seven B. thuringiensis and one B. cereus; and five Staphylococcus spp. Interestingly, with Vietnamese fish sauces, we mostly identified species of B. thuringiensis and Staphylococcus spp., while with Korean fermented fish products, the majority of the strains identified belonged to L. lactis. Among the strains, B. thuringiensis LH2134 produced the highest levels of GABA at 366 mM among the strains identified from Vietnamese fish sauces, whereas L. lactis LA43, a new strain isolated from Korean jeotgal (salted shrimp paste), produced the highest amount of GABA at 454 mM and the glutamate concentration in the medium was essential for GABA accumulation. Therefore, such the isolates might serve as good starters for development of more GABA-reinforced foods among fermented fish products.
Full-Text
Key_wordGamma-aminobutyric acid, Bacillus, fermented fish products, glutamate, lactic acid bacteria, Staphylococcus
References
  1. Y ongsawatdigul J, Rodtong S, Raksakulthai N. 2007. Acceleration of Thai fish sauce fermentation using proteinases and bacterial starter cultures. J. Food Sci. 72: M382-390.
  2. P ark J-N, Watanabe T, Endoh K-I, Watanabe K, Abe H. 2002. Taste-active components in a Vietnamese fish sauce. Fish. Sci. 68: 913-920.
  3. Nomu ra M, Nakajima I, Fujita Y, Kobayashi M, Kimoto H, Suzuki I, et al. 1999. Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145 (Pt 6): 13751380.
  4. Diana M, Quílez J, Rafecas M. 2014. Gamma-aminobutyric acid as a bioactive compound in foods: a review. J. Funct. Foods 10: 407-420.
    CrossRef
  5. K leinrok Z, Matuszek M, Jesipowicz J, Matuszek B, Opolski A, Radzikowski C. 1998. GABA content and GAD activity in colon tumors taken from patients with colon cancer or from xenografted human colon cancer cells growing as s.c. tumors in athymic nu/nu mice. J. Physiol. Pharmacol. 49: 303-310.
  6. Br aun M, Ramracheya R, Bengtsson M, Clark A, Walker JN, Johnson PR, et al. 2010. Gamma-aminobutyric acid (GABA) is an autocrine excitatory transmitter in human pancreatic beta-cells. Diabetes 59: 1694-1701.
  7. Saikusa T, Horino T, Mori Y. 1994. Accumulation of γaminobutyric acid (Gaba) in the rice germ during water soaking. Biosci. Biotech Biochem. 58: 2291-2292.
    CrossRef
  8. Shelp BJ, Bown AW, McLean MD. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 4:446-452.
    CrossRef
  9. Dhakal R , Bajpai V K, B aek K-H. 2012. Production o f gaba (γ – Aminobutyric acid) by microorganisms: A review. Braz. J. Microbiol. 43: 1230-1241.
    Pubmed CrossRef Pubmed Central
  10. Li H, Gao D, Cao Y, Xu H. 2008. A high γ-aminobutyric acid-producing Lactobacillus brevis isolated from Chinese traditionalpaocai. Ann. Microbiol. 58: 649-653.
    CrossRef
  11. H uang 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*supported by the National Natural Science Foundation of C hina (No. 30570411) a nd t he R esearch Plan o f Zhejiang Province, China. Chinese J. Chem. Eng. 15: 157-161.
  12. Park KB, Oh SH. 2007. Production of yogurt with enhanced levels of gamma-aminobutyric acid and valuable nutrients using lactic acid bacteria and germinated soybean extract. Bioresour. Technol. 98: 1675-1679.
    Pubmed CrossRef
  13. 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.
    Pubmed CrossRef
  14. Sira gusa S, De Angelis M, Di Cagno R, 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.
  15. K omatsuzaki N, Shima J, Kawamoto S, Momose H, Kimura T. 2005. Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22: 497-504.
  16. N omura 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.
  17. La Anh N. 2015. Health-promoting microbes in traditional Vietnamese fermented foods: A review. Food Science and Human Wellness 4: 147-161.
    CrossRef
  18. 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 CrossRef Pubmed Central
  19. 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
  20. Lu X, Chen Z, Gu Z, Han Y. 2008. Isolation of γ-aminobutyric acid-producing bacteria and optimization of fermentative medium. Biochem. Eng. J. 41: 48-52.
    CrossRef
  21. Gibson LF, Khoury JT. 1986. Storage and survival of bacteria by ultra-freeze. Lett. Appl. Microbiol. 3: 127-129.
    CrossRef
  22. M cDonald LC, McFeeters RF, Daeschel MA, Fleming HP. 1987. A differential medium for the enumeration of homofermentative and heterofermentative lactic acid bacteria. Appl. Environ. Microbiol. 53: 1382-1384.
  23. De Man JC, Rogosa M, Elisabeth Sharpe M. 1960. A medium for the cultivation of Lactobacilli. J. Appl. Bact. 23: 130-135.
    CrossRef
  24. Holdiness MR. 1983. Chromatographic analysis of glutamic acid decarboxylase in biological samples. J. Chromatogr. B. 277: 1-24.
    CrossRef
  25. Kim M-J, Kim K-S. 2012. Isolation and identification of γ-aminobutyric acid (GABA)-producing lactic acid bacteria from Kimchi. J. Korean. Soc. Appl. Bi. 55: 777-785.
    CrossRef
  26. R ossetti V, Lombard A. 1996. Determination of glutamate decarboxylase by high-performance liquid chromatography. J. Chromatogr. B. Biomed. Appl. 681: 63-67.
  27. Thwe SM, Kobayashi T, Luan T, Shirai T, Onodera M, Hamada-Sato N, et al. 2011. Isolation, characterization, and utilization of γ-aminobutyric acid (GABA)-producing lactic acid bacteria from Myanmar fishery products fermented with boiled rice. Fish. Sci. 77: 279-288.
    CrossRef
  28. Benso n DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL. 2002. GenBank. Nucleic Acids Res. 30: 17-20.
  29. Ya mada S, Ohashi E, Agata N, Venkateswaran K. 1999. Cloning and nucleotide sequence analysis of gyrB of Bacillus cereus, B. thuringiensis, B. mycoides, and B. anthracis and their application to the detection of B. cereus in rice. Appl. Environ. Microbiol. 65: 1483-1490.
  30. M anzano M, Giusto C, Iacumin L, Cantoni C, Comi G. 2003. A molecular method to detect Bacillus cereus from a coffee concentrate sample used in industrial preparations. J. Appl. Microbiol. 95: 1361-1366.
  31. As ano SI, Nukumizu Y, Bando H, Iizuka T, Yamamoto T. 1997. Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol. 63: 10541057.
  32. Ya ng IC, Shih DY-C, Huang T-P, Huang Y-P, Wang J-Y, Pan T-M. 2005. Establishment of a novel multiplex PCR assay and detection of toxigenic strains of the species in the Bacillus cereus group. J. Food Protect. 68: 2123-2130.
  33. Gh elardi E, Celandroni F, Salvetti S, Barsotti C, Baggiani A, Senesi S. 2002. Identification and characterization of toxigenic Bacillus cereus isolates responsible for two food-poisoning outbreaks. FEMS Microbiol. Lett. 208: 129-134.
  34. Kuo WS, Chak KF. 1996. Identification of novel cry-type genes from Bacillus thuringiensis strains on the basis of restriction fragment length polymorphism of the PCRamplified DNA. Appl. Environ. Microbiol. 62: 1369-1377.
    Pubmed Pubmed Central
  35. Gu o S, Liu M, Peng D, Ji S, Wang P, Yu Z, et al. 2008. New strategy for isolating novel nematicidal crystal protein genes from Bacillus thuringiensis strain YBT-1518. Appl. Environ. Microbiol. 74: 6997-7001.
  36. E l Sanousi SM, B. Said KB, Elbager S, Awad A, Rodwan K, Eltom KH. 2015. A flow chart for the identification of Staphylococcus species. UK J. Vet. Med. Anim. Prod. 6: 93-97.
  37. L ee YD, Moon BY, Park JH, Chang HI, Kim WJ. 2007. Expression of enterotoxin genes in Staphylococcus aureus isolates based on mRNA analysis. J. Microbiol. Biotechnol. 17:461-467.
  38. Brakstad OG, Aasbakk K, Maeland JA. 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of t he n uc g ene. Eur. J. Clin. Microbiol. 30:1654-1660.
  39. K obayashi T, Kajiwara M, Wahyuni M, Kitakado T, Hamada-Sato N, Imada C, et al. 2003. Isolation and characterization of halophilic lactic acid bacteria isolated from “terasi” shrimp paste: a traditional fermented seafood product in Indonesia. J. Gen. Appl. Microbiol. 49: 279-286.
  40. C ho GS, Do HK. 2006. Isolation and identification of lactic acid bacteria isolated from a traditional jeotgal product in Korea. Ocean. Sci. J. 41: 113-119.
  41. Saisithi P. 1994. Traditional fermented fish: fish sauce production, pp. 111-131. In Martin AM (ed.), Fisheries Processing: Biotechnological applications, Ed. Springer US, Boston, MA, USA
  42. B arla F, Koyanagi T, Tokuda N, Matsui H, Katayama T, Kumagai H, et al. 2 016. The γ-aminobutyric acid-producing ability under low pH conditions of lactic acid bacteria isolated from traditional fermented foods of Ishikawa Prefecture, Japan, with a strong ability to produce ACEinhibitory peptides. Biotechnol. Rep. 10: 105-110.
  43. Crisan EV, Sands A. 1975. Microflora of four fermented f ish sauces. Appl. Microbiol. 29: 106-108.
    Pubmed Pubmed Central
  44. Savadogo A, Ouattara CAT, Traore AS. 2007. Potential of lactic acid bacteria in human nutrition. Food 1: 79-84.
  45. Thwaite JE, Atkins HS. 2012. 21 - Bacillus: Anthrax; food poisoning A2 - Greenwood, David, pp. 237-244. In Barer M, Slack R, Irving W (eds.), Medical Microbiology (Eighteenth Edition), Ed. Churchill Livingstone, Edinburgh, UK.
  46. Sa isithi P, Kasemsarn RO, Liston J, Dollar Alexander M. 1966. Microbiology and chemistry of fermented fish. J. Food. Sci. 31: 105-110.
  47. I brahim MA, Griko N, Junker M, Bulla LA. 2010. Bacillus thuringiensis: a genomics and proteomics perspective. Bioeng. Bugs. 1: 31-50.
  48. T anasupawat S, Hashimoto Y, Ezaki T, Kozaki M, Komagata K. 1992. Staphylococcus piscifermentans sp. nov., from fermented fish in Thailand. Int. J. Syst. Bacteriol. 42:577-581.
    Pubmed CrossRef
  49. Id a Muryany MY, Ina Salwany MY, Ghazali AR, Hing HL, Nor Fadilah R. 2017. Identification and characterization of the lactic acid bacteria isolated from Malaysian fermented fish (Pekasam). Int. Food. Res. J. 24: 868-875.
  50. Za reian M, Ebrahimpour A, Bakar FA, Mohamed AKS, Forghani B, Ab-Kadir MSB, et al. 2012. A glutamic acidproducing lactic acid bacteria isolated from Malaysian fermented foods. Int. J. Mol. Sci. 13: 5482-5497.
  51. Lim HS, Cha IT, Roh SW, Shin HH, Seo MJ. 2017. Enhanced production of gamma-aminobutyric acid by optimizing culture conditions of Lactobacillus brevis HYE1 isolated from kimchi, a Korean fermented food. J. Microbiol. Biotechnol. 27:450-459.
    Pubmed CrossRef



Copyright © 2009 by the Korean Society for Microbiology and Biotechnology.
All right reserved. Mail to jmb@jmb.or.kr
Online ISSN: 1738-8872    Print ISSN: 1017-7825    Powered by INFOrang.co., Ltd