Characterization of Gamma Aminobutyric Acid-producing Lactic Acid Bacteria Isolated from Budu Fish in Padang Pariaman West Sumatra Indonesia and their Potentials as Probiotics
Applied Food Biotechnology,
Vol. 10 No. 4 (2023),
25 September 2023
,
Page 257-270
https://doi.org/10.22037/afb.v10i4.42951
Abstract
Abstract
Background and Objective: Screening of lactic acid bacteria for the production of gamma-amino-butyric acid is important due to its pharmacological functions. In this study, isolation and characterization of lactic acid bacteria from Budu fish, an endemic fish to West Sumatra, Indonesia, have been investigated and their gamma amino butyric acid-producing potentials were identified
Material and Methods: The research method was as follows: lactic acid bacteria was isolated from Budu fish bought randomly from a traditional market in West Sumatra, Indonesia. Isolates were characterized morphologically and biochemically. Gram+ isolates were investigated for their capability to produce gamma-amino-butyric acid using thin-layer chromatography. Gamma-amino-butyric acid-positive strains were quantitatively analyzed using spectrometry method. Of the five samples, the highest gamma-amino-butyric acid production was reported in one sample of IB2C isolate. The selected isolates of lactic acid bacteria were molecularly identified using 16S rRNA gene sequencing. Effects of incubation time (20, 40 and 60 h) and monosodium glutamate concentrations (2, 4 and 6%) were investigated on gamma-amino-butyric acid-production strains.
Results and Conclusion: Three isolates were selected for the production of gamma-amino-butyric acid in de Mann Rogosa Sharpe broth containing 1% monosodium glutamate. Semiquantitative analysis via pre-staining paper chromatography was carried out to identify the highest gamma amino butyric acid-producing lactic acid bacteria. The highest gamma-amino-butyric acid level of 22.5 mg.ml-1 was achieved using 60 h of incubation and 6% of monosodium glutamate concentration in de Mann Rogosa Sharpe broth. The IB2c isolates were Gram+, catalase-, homofermentative and able to utilize various carbon sources. It inhibited growth of Escherichia coli O157, Staphylococcus aureus and Salmonella enteritidis. The IB2C was further characterized molecularly using 16S rRNA sequencing gene. Results were identified as Lentilactobacillus parabuchneri strain M1-40. A 97.69% similarity of lactic acid bacteria isolated from Budu fish with Lentilactobacillus. parabuchneri indicates probiotic use of the gamma-amino butyric acid-producing lactic acid bacteria
How to Cite
References
References
Bover-Cid S, Holzapfel WH. improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol. 1999; 53(1):33-41.
https://doi.org/10.1016/S0168- 1605(99)00152-X
Song M, Yun B, Moon J-H, Park D-J, Lim K, Oh S. Characterization of selected Lactobacillus strains for use as probiotics. Korean J Food Sci Anim Resour. 2015; 35(4):551.
https://doi.org/ 10.5851/kosfa.2015.35.4.551
Sahab NRM, Subroto E, Balia RL, Utama GL. γ-Aminobutyric acid found in fermented foods and beverages: Current trends. Heliyon. 2020; 6(11):1-7
https://doi.org/10.1016/j.heliyon.2020.e05526
Yogeswara IBA, Maneerat S, Haltrich D. Glutamate decarboxylase from lactic acid bacteria-A key enzyme in GABA synthesis. Microorganisms 2020; 8 (12): 1923.
https://doi.org/10.3390/microorganisms8121923
Diana M, Quílez Z, Rafecas M. Gamma-aminobutyric acid as a bioactive compound in foods: Review. J Funct Foods. 2014; 10: 407-420.
https://doi.org/10.1016/j.jff.2014.07.004
Pramai P, Thanasukarn P, Thongsook T, Jannoey P, Chen F, Jiamyangyuen S. Glutamate decarboxylase (GAD) extracted from germinated rice: Enzymatic properties and its application in soymilk. J Nutr Sci Vitaminol. 2019; 65: 166-170.
https://doi.org/10.3177/jnsv.65.S166
Cui Y, Miao K, Niyaphorn S, Qu X. Production of gamma-aminobutyric acid from lactic acid bacteria: A systematic review. Int J Mol Sci. 2020; 21 (3): 955.
https://doi.org/10.3390/ijms21030995
Choat HM. Effect of gamma aminobutyric acid (GABA) or GABA with glutamic acid decarboxylase (GAD) on the progression of type 1 diabetes mellitus in children: Trial design and methodology. Contemp Clin Trials. 2019; 82: 93-100.
https://doi.org/10.1016/j.cct.2019.06.007
Ly D, Mayrhofer S, Agung Yogeswara IB, Nguyen T-H, Domig KJ. Identification, classification and screening for γ-amino-butyric acid production in lactic acid bacteria from Cambodian fermented foods. Biomolecules. 2019; 9(12):768.
https://doi.org/10.3390/biom9120768
Li Y, Chen X, Shu G, Ma W. Screening of gamma-aminobutyric acid-producing lactic acid bacteria and its application in Monascus-fermented rice production. Acta Sci Pol Technol Aliment. 2020; 19 (4):387-394.
https://doi.org/10.17306/J.AFS.2020.0868
Kanklai J, Somwong TC, Rungsirivanich P, Thongwai N. Screening of GABA-producing lactic acid bacteria from Thai fermented foods and probiotic potential of Levilactobacillus brevis F064A for GABA-fermented mulberry juice production. Microorganisms 2020; 9 (1): 33.
https://doi.org/10.3390/microorganisms9010033
Hwang E, Park J-Y. Isolation and characterization of gamma-aminobutyric acid (GABA)-producing lactic acid bacteria from kimchi. Curr Top Lact Acid Bact Probiotics 2020; 6(2); 64-69.
https://doi.org/10.35732/ctlabp.2020.6.2.64
Galli V, Enturi M, Mari E, Guerrini S, Granchi L. Gamma-aminobutyric acid (GABA) production in fermented milk by lactic acid bacteria isolated from spontaneous raw milk fermentation. Int Dairy J. 2020; 127; 105284.
https://doi.org/10.1016/j.idairyj.2021.105284
Komatsuzaki N, Shima J, Kawamoto S, Momose H, Kimura T. Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 2005; 22(6): 497-504.
https://doi.org/10.1016/j.fm.2005.01.002
Phuengjayaem S, Booncharoen A, Tanasupawat S. Characteriz-ation and comparative genomic analysis of gamma-aminobutyr-ic acid (GABA)-producing lactic acid bacteria from Thai fermented foods. Biotechnol Lett. 2021; 43(8): 1637-1648.
https://doi.org/10.1007/s10529-021-03140-y
Kook M-C, Cho S-C. Production of GABA (gamma amino butyric acid) by lactic acid bacteria. Kor J Food Sci Anim Resour. 2013; 33(3): 377-389.
http://dx.do.org/10.5851/kosfa.2013.33.3.377
Guevara EE, Frankel Dc, Ranaivonasy J, Richard AF, Ratsirarson J, Lawler RR, Bradley BJ. A simple economical protocol for DNA extraction and amplification where there is no lab. Conserv Genet Resour. 2018; 10:119-1245.
https://doi.org/10.1007/s12686-017-0758-5
Mohamed HN, Man YC, Mustafa S, Manap YA, Tentative identification of volatile flavor compounds in commercial budu, a Malaysian fish sauce, using GC-MS. Molecules 2012;17 (5):5062-5080.
https://doi.org/10.3390/molecules17055062
Prima HS, Endang P, Rusfidra. Isolation, characterization and identification of molecular lactic acid is isolated from bilih fish (Mystacoleucus padangensis) lake singkarak potential as a probiotic. Ann Rom Soc Cell Biol. 2021: 8581-8596.
Song J, Peng S, Yang J, Zhou F, Suo H. Isolation and identification of novel antibacterial peptides produced by Lactobacillus fermentum SHY10 in Chinese pickles. Food Chem. 2021; 348: 129097.
https://doi.org/10.1016/j.foodchem.2021.129097
Rayavarapu B, Tallapragada P. Optimization and comparison of ℽ-aminobutyric acid (GABA) production by LAB in soymilk using RSM and ANN models. Beni-Suef Univ J Basic Appl Sci. 2021;10: 1-15.
https://doi.org/10.1186/s43088-021-00100-3
Silberbauer LR.. Effect of ketamine on limbic GABA and glutamate: A human in vivo multivoxel magnetic resonance spectroscopy study. Front Psychiatry. 2020; 11: 549903.
https://doi.org/10.3389/fpsyt.2020.549903
Prima HS, Satrianto A, Amar S. Antimicrobial potential of Limosilactobacillus Fermentum isolated from bilih fish (Mystacoleucus padangensis) of singkarak lake, west sumatera, indonesia. Appl Food Biotechnol. 2022; 9(4): 297-309.
https://doi.org/10.22037/afb.v9i4.38487
Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR. Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. Plos One. 2018; 13(3): 0192978.
https://doi.org/10.1371/journal.pone.0192978
Siddiq MMA, Pramudia D, Nefilinda N, Syukriani L, Jamsari. Metagenomic Profile of Endophytic Bacteria in Acacia Mearnsii. in IOP Conference Series: Earth and Environmental Science, IOP Publishing. 2023: 12030.
https://doi.org/10.1186/s13213-020-01542-3
Santos-Espinosa A. Gamma-aminobutyric acid (GABA) production in milk fermented by specific wild lactic acid bacteria strains isolated from artisanal Mexican cheeses. Ann Microbiol. 2020; 70 (1): 1-11.
https://doi.org/10.1186/s13213-020-01542-3
Yu P, Ren Q, Wang X, Huang X. Enhanced biosynthesis of γ-aminobutyric acid (GABA) in Escherichia coli by pathway engineering. Biochem Eng J. 2019; 141: 252-258.
https://doi.org/10.1016/j.bej.2018.10.025
Shi F, Ni Y, Wang N. Metabolism and biotechnological production of gamma‐aminobutyric Acid (GABA), In: Ind Biotechnol Vitamins Biopigments Antioxidants, Editors: Van Damme EJ, Revuelta JL. Wiley-VCH; 1st edition: 2016: 445-468.
https://doi.org/10.1002/9783527681754.ch16
Xu J, Zhang Q, Li D, Du D, Wang C, Qin J. Rapid degradation of long-chain crude oil in soil by indigenous bacteria using fermented food waste supernatant. Waste Manag. 2019;85:361-373.
https://doi.org/10.1016/j.wasman.2018.12.041
Rashmi D, Zanan R, John S, Khandagale K, Nadaf A. γ-aminobutyric acid (GABA): Biosynthesis, role, commercial production, and applications. Stud Nat Prod Chem. 2018;57: 413-452.
https://doi.org/10.1016/B978-0-444-64057-4.00013-2
Sanchart C, Rattanaporn O, Haltrich D , Phukpattaranont P, Maneerat S, Lactobacillus futsaii CS3, a new GABA-producing strain isolated from Thai fermented shrimp (Kung-Som). Indian J Microbiol. 2017; 57: 211-217.
https://doi.org/10.1007/s12088-016-0632-2
Tanamool V, Hongsachart P, Soemphol W. Screening and characterization of gamma-aminobutyric acid (GABA) producing lactic acid bacteria isolated from Thai fermented fish (Plaa-som) in Nong Khai and its application in Thai fermented vegetables (Som-pak). Food Sci Technol. 2019; 40: 483-490.
https://doi.org/10.1590/fst.05419
Vo TT-T, Park J-H. Characteristics of potential gamma-aminobutyric acid-producing bacteria isolated from Korean and Vietnamese fermented fish products. Microbiol Biotechnol. 2019; 29(2): 209-271
https://doi.org/10.4014/jmb.1811.09072
Moe NKT, Thwe SM, Shirai T, Terahara T, Imada C, Kobayashi T. Characterization of lactic acid bacteria distributed in small fish fermented with boiled rice in Myanmar. Fish Sci. 2015;81;373-381.
https://doi.org/10.1007/s12562-014-0843-6
Ma Y, Wang P, Chen Z, Gu Z, Yang R. GABA enhances physio-biochemical metabolism and antioxidant capacity of germinated hulless barley under NaCl stress. J Plant Physiol. 2018; 231: 192-201.
https://doi.org/10.1016/j.jplph.2018.09.015
Thaler MD, Franziska S, Anna L, Thaller MSC, Christoph F, Kumpfel MD, et al. Abundant glutamic acid decarboxylase (GAD)-reactive B cells in gad‐antibody-associated neurologic-al disorders. Ann Neurol. 2019; 85(3): 448-454.
https://doi.org/10.1002/ana.25414
Thwe SM, Kobayashi, Luan T, shirai T, Onodera M, Sato NH, Imada C. Isolation, characterization, and utilization of γ-aminobutyric acid (GABA)-producing lactic acid bacteria from Myanmar fishery products fermented with boiled rice. Fish Sci. 2011; 77: 279-288.
https://doi.org/10.1007/s12562-011-0328-9
You S, Du S, Ge G, Wan T, Jia T. Microbial community and fermentation characteristics of native grass prepared without or with isolated lactic acid bacteria on the mongolian plateau. Front Microbiol. 2021; 12: 731770.
https://doi.org10.3389/fmicb.2021.731770
Chen SU, Chen L, Chen L, Ren X, Ge H, Li B, Ma G, K X, Zhu J, Li L, Feng Y, Li Y. Potential probiotic characterization of Lactobacillus reuteri from traditional Chinese highland barley wine and application for room-temperature-storage drinkable yogurt. J Dairy Sci. 2018; 101(7): 5780-5788.
https://doi.org/10.3168/jds.2017-14139
Sokovic BS, GABA-producing natural dairy isolate from artisanal zlatar cheese attenuates gut inflammation and strengthens gut epithelial barrier in vitro. Front Microbiol. 2019; 10: 527.
https://doi.org/10.3389/fmicb.2019.00527
Da Costa RJ, Silva AP, Nalerio ES, Fonseca RN, Hubner SO, Nalerio ES, et all. Characterization of Enterococcus faecium EO1 isolated from mutton and activity of bacteriocin-like substances in the control of Listeria monocytogenes in fresh mutton sausage. LWT. 2021;141:110954.
https://doi.org/10.3168/jds.2017-14139
Bungenstock L, Abdulmawjood A, Reich F. Evaluation of antibacterial properties of lactic acid bacteria from traditionally and industrially produced fermented sausages from Germany. Plos One. 2020; 15(3): e0230345.
https://doi.org/10.1371/journal.pone.0230345
Amarantini C, Satwika D, Budiarso YT, Yunita ER, Laheba EA. Screening of antimicrobial-producing lactic acid bacteria isolated from traditional fish fermentation against pathogenic bacteria. J Physics: Conference Series, IOP Publishing. 2019: 12045.
https://doi.org/10.1088/1742-6596/1397/1/012045
Jia B, Pu ZJ, Tang K, Jia x, K k, Liu X, J CO. Catalytic, computational, and evolutionary analysis of the D-lactate dehydrogenases responsible for D-lactic acid production in lactic acid bacteria. J Agric Food Chem. 2018; 66(31): 668371-8381.
https://doi.org/10.1021/acs.jafc.8b02454
Zhang Y, et al., Bio-protective potential of lactic acid bacteria: Effect of Lactobacillus sakei and Lactobacillus curvatus on changes of the microbial community in vacuum-packaged chilled beef. Asian-Australasian J Anim Sci. 2018; 31(4): 585.
https://doi.org/10.5713/ajas.17.0540
Matti A, Utami T, Hidayat C, Rahayu ES. Isolation, Screening, and identification of proteolytic lactic acid bacteria from indigenous Chao product. J Aquat Food Prod Technol. 2019; 28(7): 781-793.
https://doi.org/10.1080/10498850.2019.1639872
Liang N, Zhao Z, Curtis JM, Ganzle MG. Antifungal cultures and metabolites of lactic acid bacteria for use in dairy fermentations. Int J Food Microbiol. 2022; 383: 109938.
https://doi.org/10.1016/j.ijfoodmicro.2022.109938
Yang B, Wang Y, Qian P-Y. Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformatics. 2016;17(1):1-8.
https://doi.org/10.1186/s12859-016-0992-y
Huang CH, Li WS, Huang L, Watanabe K, Identification and classification for the Lactobacillus casei group. Front. Microbiol. 2018;9: 1974.
https://doi.org/10.3389/fmicb.2018.01974
Vasile MA, Jeiter J, Weigend M, Luebert F. Phylogeny and historical biogeography of Hydrophyllaceae and Namaceae, with a special reference to Phacelia and Wigandia. Syst Biodivers. 2020; 18(8): v757-770.
https://doi.org/10.1080/14772000.2020.1771471
Tofalo R, Perpetuini G, Battistelli N, Pepe A, Lanni A, Martino G, Suzzi G. Accumulation γ-aminobutyric acid and biogenic amines in a traditional raw milk ewe’s cheese. Food. 2019; 8(9): 401.
https://doi.org/10.3390/foods8090401
Botello-Morte L, Moniente M, Gil-Ramírez Y, Virto R, García-Gonzalo D, Pagan R. Identification using molecular tools of the microbiota responsible for the formation of histamine accumulated in commercial cheeses in Spain. Food Control. 2022; 133: 108595.
https://doi.org/10.1016/j.foodcont.2021.108595
Wang D, Liu W, Ren Y, De L, Yang Y, Bao Q, Zhang H, Menghe B. Isolation and identification of lactic acid bacteria from traditional dairy products in Baotou and bayannur of midwestern inner mongolia and q-PCR analysis of predominant species. Korean J food Sci Anim Resour. 2016; 34(4): 499.
- Abstract Viewed: 250 times
- pdf Downloaded: 207 times