Isolation and Selection of Lactic Acid Bacteria with the Capacity of Producing γ-aminobutyric Acid (GABA) and Antimicrobial Activity: Its Application in Fermented Meat Product

Page: [831 - 837] Pages: 7

  • * (Excluding Mailing and Handling)

Abstract

Background: γ-aminobutyric acid produced from lactic acid bacteria can be an ideal component in food products due to its health functional properties.

Objective: This study aimed to isolate lactic acid bacteria (LAB) with the capacity of producing γ-aminobutyric acid (GABA) and evaluated its antimicrobial activities and application of Nem Chua (the traditionally fermented meat product).

Methods: LAB strains from 7 types of Nem Chua products were isolated and evaluated for their GABA-producing and antibacterial capacities. The Nem Chua product was prepared from the selected GABA-producing LAB strain and evaluated for its GABA content, pH, and lactic acid levels.

Results: Six strains (CP2, HC2, LV2, TP1, VL1, and XP1) were isolated being capable of producing GABA (1.234 – 1.568 mg/ml) after 24 h of fermentation. Among them, the strain VL1 was found to produce the highest GABA content and induce the highest antimicrobial activity against Bacillus Subtilis (19.7 mm in zone inhibition diameter). Strain VL1 was identified as Lactobacillus Plantarum and was used for the production of Nem Chua, which was found to contain 1.103 mg/g of GABA and 22 mg/g of lactic acid.

Conclusion: The result showed the high feasibility of using GABA-producing strain L. Plantarum VL1 to develop functional products due to its health-beneficial effects.

Graphical Abstract

[1]
Liu W, Pang H, Zhang H, Cai Y. Biodiversity of lactic acid bacteria. In: Zhang H, Cai Y, Eds. Lactic Acid Bacteria. Berlin: Springer 2014; pp. 103-203.
[http://dx.doi.org/10.1007/978-94-017-8841-0_2]
[2]
Hwanhlem N, Watthanasakphuban N, Riebroy S, Benjakul S. H-Kittikun A, Maneerat S. Probiotic lactic acid bacteria from Kung-Som: Isolation, screening, inhibition of pathogenic bacteria. Int J Food Sci Technol 2010; 45(3): 594-601.
[http://dx.doi.org/10.1111/j.1365-2621.2010.02172.x]
[3]
Franciosi E, Carafa I, Nardin T, et al. Biodiversity and γ-aminobutyric acid production by lactic acid bacteria isolated from traditional alpine raw cow’s milk cheeses. BioMed Res Int 2015; 2015: 1-11.
[http://dx.doi.org/10.1155/2015/625740]
[4]
Diana M, Quílez J, Rafecas M. Gamma-aminobutyric acid as a bioactive compound in foods: A review. J Funct Foods 2014; 10: 407-20.
[http://dx.doi.org/10.1016/j.jff.2014.07.004]
[5]
Okada T, Sugishita T, Murakami T, et al. Effect of the defatted rice germ enriched with GABA for sleeplessness, depression, autonomic disorder by oral administration. Nippon Shokuhin Kagaku Kogaku Kaishi 2000; 47(8): 596-603.
[http://dx.doi.org/10.3136/nskkk.47.596]
[6]
Abdou AM, Higashiguchi S, Horie K, Kim M, Hatta H, Yokogoshi H. Relaxation and immunity enhancement effects of γ-Aminobutyric acid (GABA) administration in humans. Biofactors 2006; 26(3): 201-8.
[http://dx.doi.org/10.1002/biof.5520260305] [PMID: 16971751]
[7]
Inoue K, Shirai T, Ochiai H, et al. Blood-pressure-lowering effect of a novel fermented milk containing γ-aminobutyric acid (GABA) in mild hypertensives. Eur J Clin Nutr 2003; 57(3): 490-5.
[http://dx.doi.org/10.1038/sj.ejcn.1601555] [PMID: 12627188]
[8]
Lin SD, Mau JL, Hsu CA. Bioactive components and antioxidant properties of γ-aminobutyric acid (GABA) tea leaves. Lebensm Wiss Technol 2012; 46(1): 64-70.
[http://dx.doi.org/10.1016/j.lwt.2011.10.025]
[9]
Chuang CY, Shi YC, You HP, Lo YH, Pan TM. Antidepressant effect of GABA-rich monascus-fermented product on forced swimming rat model. J Agric Food Chem 2011; 59(7): 3027-34.
[http://dx.doi.org/10.1021/jf104239m] [PMID: 21375324]
[10]
Di Cagno R, Mazzacane F, Rizzello CG, et al. Synthesis of γ-aminobutyric acid (GABA) by Lactobacillus plantarum DSM19463: Functional grape must beverage and dermatological applications. Appl Microbiol Biotechnol 2010; 86(2): 731-41.
[http://dx.doi.org/10.1007/s00253-009-2370-4] [PMID: 20013120]
[11]
Yu J, Wang WH, Menghe BLG, et al. Diversity of lactic acid bacteria associated with traditional fermented dairy products in Mongolia. J Dairy Sci 2011; 94(7): 3229-41.
[http://dx.doi.org/10.3168/jds.2010-3727] [PMID: 21700007]
[12]
Nuraida L. A review: Health promoting lactic acid bacteria in traditional Indonesian fermented foods. Food Sci Hum Wellness 2015; 4(2): 47-55.
[http://dx.doi.org/10.1016/j.fshw.2015.06.001]
[13]
Thapa N, Pal J, Tamang JP. Microbial diversity in ngari, hentak and tungtap, fermented fish products of North-East India. World J Microbiol Biotechnol 2004; 20(6): 599-607.
[http://dx.doi.org/10.1023/B:WIBI.0000043171.91027.7e]
[14]
Nguyen DTL, Van Hoorde K, Cnockaert M, et al. A culture-dependent and independent approach for the identification of lactic acid bacteria associated with the production of nem chua, a Vietnamese fermented meat product. Food Res Int 2013; 50(1): 232-40.
[http://dx.doi.org/10.1016/j.foodres.2012.09.029]
[15]
Khunajakr N, Wongwicharn A, Moonmangmee D, Tantipaiboonvut S. Screening and identification of lactic acid bacteria producing antimicrobial compounds from pig gastrointestinal tracts. Curr Appl Sci Technol 2008; 8(1): 8-17.
[16]
Axelsson L. Lactic acid bacteria: classification and physiology. In: Salminen S, von Wright A, Eds. Lactic Acid Bacteria: Microbiological and Functional Aspects. Florida: CRC Press 2004; 139: pp. 1-66.
[http://dx.doi.org/10.1201/9780824752033.ch1]
[17]
Li H, Qiu T, Cao Y, Yang J, Huang Z. Pre-staining paper chromatography method for quantification of γ-aminobutyric acid. J Chromatogr A 2009; 1216(25): 5057-60.
[http://dx.doi.org/10.1016/j.chroma.2009.04.044] [PMID: 19446298]
[18]
Annuk H, Shchepetova J, Kullisaar T, Songisepp E, Zilmer M, Mikelsaar M. Characterization of intestinal lactobacilli as putative probiotic candidates. J Appl Microbiol 2003; 94(3): 403-12.
[http://dx.doi.org/10.1046/j.1365-2672.2003.01847.x] [PMID: 12588549]
[19]
Hütt P, Shchepetova J, Lõivukene K, Kullisaar T, Mikelsaar M. Antagonistic activity of probiotic lactobacilli and bifidobacteria against entero and uropathogens. J Appl Microbiol 2006; 100(6): 1324-32.
[http://dx.doi.org/10.1111/j.1365-2672.2006.02857.x] [PMID: 16696680]
[20]
Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173(2): 697-703.
[http://dx.doi.org/10.1128/jb.173.2.697-703.1991] [PMID: 1987160]
[21]
Nhung NTM. Research on improving production and preservation techniques to improve the quality of spring rolls 2005.
[22]
Le TM, Nguyen TH, Pham TT, Nguyen TH, Le TLC. Analytical methods in fermentation technology. Vietnam: Sci Technol Publ House 2006.
[23]
The Firmicutes 3rd ed Vos P Garrity G Jones D et al Bergey’s manual of systematic bacteriology Berlin. Springer Science & Business Media 2011; p. 3.
[24]
TCVN. Non - Heat treated processed meat – Specification Available from: https://vanbanphapluat.co/tcvn-7050-2002-thit-che-bien-khong-qua-xu-ly-nhiet-quy-dinh-ky-thuat (Accessed on: June 2022).
[25]
Yien Ong Y, Siang Tan W, Rosfarizan M, Chan ES, Ti Tey B. Isolation and identification of lactic acid bacteria from fermented red dragon fruit juices. J Food Sci 2012; 77(10): M560-4.
[http://dx.doi.org/10.1111/j.1750-3841.2012.02894.x]
[26]
Mulaw G, Sisay TT, Muleta D, Tesfaye A. In vitro evaluation of probiotic properties of lactic acid bacteria isolated from some traditionally fermented ethiopian food products. Int J Microbiol 2019; 2019: 1-11.
[http://dx.doi.org/10.1155/2019/7179514]
[27]
Park SY, Lee JW, Lim SD. The probiotic characteristics and GABA production of Lactobacillus plantarum K154 isolated from kimchi. Food Sci Biotechnol 2014; 23(6): 1951-7.
[http://dx.doi.org/10.1007/s10068-014-0266-2]
[28]
Sokovic Bajic S, Djokic J, Dinic M, et al. GABA-producing natural dairy isolate from artisanal zlatar cheese attenuates gut inflammation and strengthens gut epithelial barrier in vitro. Front Microbiol 2019; 10: 527.
[http://dx.doi.org/10.3389/fmicb.2019.00527] [PMID: 30936860]
[29]
Liu A, Li X, Pu B, et al. Use of psychrotolerant lactic acid bacteria (Lactobacillus spp. and Leuconostoc spp.) isolated from chinese traditional paocai for the quality improvement of paocai products. J Agric Food Chem 2017; 65(12): 2580-7.
[http://dx.doi.org/10.1021/acs.jafc.7b00050] [PMID: 28276234]
[30]
Zare Mirzaei E, Lashani E, Davoodabadi A. Antimicrobial properties of lactic acid bacteria isolated from traditional yogurt and milk against Shigella strains. GMS Hyg Infect Control 2018; 13: Doc01.
[PMID: 29416958]
[31]
Cui Y, Qu X, Li H, et al. Isolation of halophilic lactic acid bacteria from traditional Chinese fermented soybean paste and assessment of the isolates for industrial potential. Eur Food Res Technol 2012; 234(5): 797-806.
[http://dx.doi.org/10.1007/s00217-012-1689-8]
[32]
Ko CY, Lin HTV, Tsai GJ. Gamma-aminobutyric acid production in black soybean milk by Lactobacillus brevis FPA 3709 and the antidepressant effect of the fermented product on a forced swimming rat model. Process Biochem 2013; 48(4): 559-68.
[http://dx.doi.org/10.1016/j.procbio.2013.02.021]
[33]
Ratanaburee A, Kantachote D, Charernjiratrakul W, Sukhoom A. Selection of γ-aminobutyric acid-producing lactic acid bacteria and their potential as probiotics for use as starter cultures in Thai fermented sausages (Nham). Int J Food Sci Technol 2013; 48(7): 1371-82.
[http://dx.doi.org/10.1111/ijfs.12098]
[34]
Barla F, Koyanagi T, Tokuda N, et al. 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 ACE-inhibitory peptides. Biotechnol Rep (Amst) 2016; 10: 105-10.
[http://dx.doi.org/10.1016/j.btre.2016.04.002] [PMID: 28352530]
[35]
Laroute V, Yasaro C, Narin W, et al. GABA production in Lactococcus lactis is enhanced by arginine and co-addition of malate. Front Microbiol 2016; 7: 1050.
[http://dx.doi.org/10.3389/fmicb.2016.01050] [PMID: 27458444]
[36]
Onda T, Yanagida F, Tsuji M, Ogino S, Shinohara T. Isolation and characterization of the lactic acid bacterial strain GM005 producing a antibacterial substance from miso-paste product. Food Sci Technol Res 1999; 5(3): 247-50.
[http://dx.doi.org/10.3136/fstr.5.247]
[37]
Ouwehand AC, Vesterlund S. Antimicrobial components from lactic acid bacteria. In: Vinderola G, Ouwehand A, Salminen S, von Wright A, Eds. Lactic Acid Bacteria: Microbiological and Functional Aspects. Florida: CRC Press 2004; 139: pp. 375-96.
[http://dx.doi.org/10.1201/9780824752033.ch11]
[38]
Barbosa MS, Jurkiewicz C, Landgraf M, Todorov SD, Franco BDGM. Effect of proteins, glucose and NaCl on growth, biosynthesis and functionality of bacteriocins of Lactobacillus sakei subsp. sakei 2a in foods during storage at 4°C: Tests in food models. Lebensm Wiss Technol 2018; 95: 167-71.
[http://dx.doi.org/10.1016/j.lwt.2018.04.082]
[39]
Trindade DPA, Barbosa JP, Martins EMF, Tette PAS. Isolation and identification of lactic acid bacteria in fruit processing residues from the Brazilian Cerrado and its probiotic potential. Food Biosci 2022; 48: 101739.
[http://dx.doi.org/10.1016/j.fbio.2022.101739]
[40]
Sakandar HA, Kubow S, Sadiq FA. Isolation and in vitro probiotic characterization of fructophilic lactic acid bacteria from Chinese fruits and flowers. Lebensm Wiss Technol 2019; 104: 70-5.
[http://dx.doi.org/10.1016/j.lwt.2019.01.038]
[41]
Corsetti A, Valmorri S. Lactic acid bacteria| Lactobacillus spp.: Lactobacillus plantarum.In: Fuquay JW, McSweeney PL, Fox PF,Eds Encyclopedia of Dairy Science. Cambridge: Academic Press 2011; pp. 111-6.
[http://dx.doi.org/10.1016/B978-0-12-374407-4.00263-6]
[42]
Yogeswara AI, Kusumawati IGAW, Sumadewi NLU, Rahayu ES, Indrati R. Isolation and identification of lactic acid bacteria from Indonesian fermented foods as γ-aminobutyric acid-producing bacteria. Int Food Res J 2018; 25(4): 1753-7.
[43]
Ly D, Mayrhofer S, Agung YI, Nguyen TH, Domig K. Identification, classification and screening for γ-amino-butyric acid production in lactic acid bacteria from cambodian fermented foods. Biomolecules 2019; 9(12): 768.
[http://dx.doi.org/10.3390/biom9120768] [PMID: 31766706]
[44]
Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M. Synthesis of γ-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol 2007; 73(22): 7283-90.
[http://dx.doi.org/10.1128/AEM.01064-07] [PMID: 17890341]
[45]
Byun JI, Shin YY, Chung SE, Shin WC. Safety and efficacy of gamma-aminobutyric acid from fermented rice germ in patients with insomnia symptoms: A randomized, double-blind trial. J Clin Neurol 2018; 14(3): 291-5.
[http://dx.doi.org/10.3988/jcn.2018.14.3.291] [PMID: 29856155]