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  • 1 Faculty of Engineering and Food Technology, Hue University of Agriculture and Forestry, Hue University, 49000, Vietnam
  • | 2 Faculty of Agriculture and Forestry, Dalat University, Dalat, 66000, Vietnam
  • | 3 School of Science, Western Sydney University, Sydney, NSW 2751, Australia
  • | 4 Laboratory of Microbiology, Department of Biochemistry and Microbiology, Ghent University, Ghent, Belgium
Open access

Abstract

Gamma-aminobutyric acid (GABA), a four-carbon non-protein amino acid, is widely known to have multiple physiological functions. The present study aimed to investigate the cultivation parameters for GABA production by a lactic acid bacteria (LAB) strain isolated from a tuna gut sample. Among 60 tuna gut LAB, only 7 Limosilactobacillus fermentum isolates, i.e. NG01, NG12, NG13, NG14, NG16, NG23, and NG27, were capable of GABA fermentation, with NG16 being the most potent GABA producer. The GABA production by isolate NG16 was therefore thoroughly characterised. The optimal batch culture conditions for GABA production were an initial cell density of 5×106 CFU mL−1, a monosodium glutamate concentration of 2%, an initial pH of 7, a fermentation temperature of 35 °C, and an incubation time of 96 h. Under this cultivation conditions, NG16 produced a maximum GABA yield of 25.52 ± 0.41 mM.

Abstract

Gamma-aminobutyric acid (GABA), a four-carbon non-protein amino acid, is widely known to have multiple physiological functions. The present study aimed to investigate the cultivation parameters for GABA production by a lactic acid bacteria (LAB) strain isolated from a tuna gut sample. Among 60 tuna gut LAB, only 7 Limosilactobacillus fermentum isolates, i.e. NG01, NG12, NG13, NG14, NG16, NG23, and NG27, were capable of GABA fermentation, with NG16 being the most potent GABA producer. The GABA production by isolate NG16 was therefore thoroughly characterised. The optimal batch culture conditions for GABA production were an initial cell density of 5×106 CFU mL−1, a monosodium glutamate concentration of 2%, an initial pH of 7, a fermentation temperature of 35 °C, and an incubation time of 96 h. Under this cultivation conditions, NG16 produced a maximum GABA yield of 25.52 ± 0.41 mM.

1 Introduction

Gamma-aminobutyric acid (GABA) is a non-protein amino acid, which is widely present in nature including animals, plants, and microorganisms. It plays an important role in the central nervous system as an inhibitory neurotransmitter that may regulate blood pressure and diuretic and tranquiliser effects (Somkuti et al., 2012). In addition, it possesses antioxidant, hypolipidemic, and anti-inflammatory properties (Diana et al., 2014). Fermentation processes can increase the GABA content in food, and recent studies have focused on the development of GABA containing functional foods (Ratanaburee et al., 2013). A variety of microorganisms can be used as starter cultures for GABA fermentation. Among these, lactic acid bacteria (LAB) are the most popular because of their GRAS (generally recognized as safe) status. Many LAB, such as Lactococcus lactis (Laroute et al., 2016), Companilactobacillus futsaii (Sanchart et al., 2017), Corynebacterium glutamicum, Lactiplantibacillus plantarum (Yang et al., 2015), and Streptococcus thermophilus (Han et al., 2020), have the capacity to produce high amounts of GABA.

The GABA production capacity of LAB depends on the specificity and activity of various intracellular enzymes. Glutamic acid decarboxylase (GAD, EC 4.1.1.15) consists of the GAD enzyme (encoded by gadA or gadB) and the glutamate/GABA antiporter GadC (Yunes et al., 2016). GABA is formed by the decarboxylation of l-glutamate transported into a cell through GadC by GAD with pyridoxal-50-phosphate (PLP) as a cofactor. GABA is then released into the culture medium by GadC. In addition, alpha-ketoglutaric acid generated in the TCA cycle is converted into l-glutamate by l-glutamate dehydrogenase (GDH, EC 1.4.1.4). Conversely, GABA can be degraded to succinic semialdehyde through the activity of GABA aminotransferase (GABA-AT, EC 2.6.1.19). This complex intracellular enzyme system results in a strain-specific GABA production activity (Cui et al., 2020), which is influenced by cultivation conditions (Sanchart et al., 2017). Therefore, scrutinous strain selection and optimisation of fermentation conditions are of paramount importance to obtain high GABA yields.

Fish sauce is a popular fermented product in Vietnam and many other Asian countries. Its production involves metabolic activities of fish gut microbiota, among which LAB play a vital role as they enhance flavour and quality of the fermented product. In the present study, we identify and optimise the cultivation conditions for GABA production by a LAB strain derived from tuna gut.

2 Materials and methods

2.1 Isolation of lactic acid bacteria

Entire gut fractions of 40 freshly caught tuna were used to isolate LAB. Samples were homogenised in Ringer's solution (Sigma-Aldrich, Milan, Italy), serially diluted, plated onto MRS agar (Oxoid, Milan, Italy), and anaerobically incubated at 37 °C for 48 h. Colonies were randomly selected, Gram stained, and catalase tested. Gram-stain-positive and catalase-negative isolates were considered to be presumptive LAB and were stored at –80 °C for further analysis.

2.2 Preparation of inoculants

LAB isolates were grown at 37 °C for 24 h in MRS broth in screw cap tubes. Cell pellets obtained after centrifuging (Universal 320R, Hettich GmbH & Co. KG, Tuttlingen, Germany) 24 h old cultures at 12,000 g for 5 min at 4 °C were resuspended in Ringer's solution. OD600 values were used to standardise cell suspensions as inoculants.

2.3 Screening of GABA-producing LAB

LAB isolates were grown for 24 h in MRS broth in screw cap tubes containing 1% (w/v) monosodium glutamate (MSG) with an initial pH of 6.2 and at 37 °C. The GABA content in the supernatant obtained after centrifuging (Universal 320R, Hettich GmbH & Co. KG, Tuttlingen, Germany) at 12,000 g for 5 min at 4 °C was analysed by HPLC as described below.

2.4 Identification of LAB isolates

Isolates were grown on MRS agar under anaerobic conditions at 37 °C for 48 h. Third-generation bacterial cells were harvested and identified following a MALDI-TOF MS method described previously (Thuy et al., 2021).

2.5 Optimisation of culture conditions for GABA production

The factors studied included MSG concentration (0, 0.5, 1, 1.5, and 2%), initial cell density (5×105, 106, 5×106, 107, and 5×107 CFU mL−1), initial pH (4, 5, 6, 7, 8, and 9), culture temperature (30, 35, 40, 45, and 50 °C), and incubation time (24, 48, 72, 96, and 120 h). When assessing the effect of one culture condition on GABA production the other factors were kept constant.

2.6 Quantification of GABA content

The supernatants obtained after centrifugation (Universal 320R, Hettich GmbH & Co. KG, Tuttlingen, Germany) of cultures at 12,000 g for 5 min at 4 °C was 10-fold diluted with deionised water. The dissolved proteins in the supernatants were removed by adding 1 mL of 3% sulfosalicylic acid and centrifuging at 6,000 r.p.m. for 5 min. GABA from the resulting supernatants was then derivatised by dabsylation with 4 mM 4-dimethylaminoazobenzen-4-sulfonyl chloride at 70 °C for 20 min and quantified by using an HPLC method as described previously (Thuy et al., 2021).

2.7 Statistical data analysis

All data are reported as mean ± SD from triplicate experiments. One-way ANOVA, Tukey's HSD and Duncan's multiple range tests were used to compare the means. A difference was considered statistically significant if P ≤ 0.05. All analyses were conducted using SPSS v. 16.0 (SPSS Inc, Chicago, IL USA).

3 Results and discussion

3.1 Screening of GABA-producing LAB

The screening of multiple LAB isolates is essential to identify GABA-producing strains. Among 60 tuna gut isolates tested, only seven, i.e. NG01, NG12, NG13, NG14, NG16, NG23, and NG27, were capable of GABA production, with NG16 as the most potent GABA producer (Fig. 1). Upon initial screening in MRS broth (comprising an initial cell density of 107 CFU mL−1, 1% monosodium glutamate, pH 6.2, 37 °C) for 24 h, the GABA content in spent culture medium produced by this NG16 isolate was 13.21 ± 0.31 mM.

Fig. 1.
Fig. 1.

GABA production by 7 lactic acid bacterium isolates. Bars with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

3.2 Identification of LAB isolates

Sixty tuna gut isolates were characterised using MALDI-TOF MS. The obtained mass spectra were compared with those of taxonomically well characterised reference strains in an in-house built reference database (Wieme et al., 2014; Lappa et al., 2021). Isolates were considered identified when their spectra clustered among taxonomically well characterised reference strains of a single LAB species, as described by Wieme et al. (2014). The mass spectra of the isolate NG16 coded as R-66963 belonged to a cluster that was assigned to Limosilactobacillus fermentum.

3.3 Effect of culture conditions on GABA production by L. fermentum NG16

3.3.1 Initial cell density

Previous studies showed that the dynamics of GABA fermentation by LAB species is greatly affected by initial cell density (Ratanaburee et al., 2013; Thuy et al., 2021). We, therefore, investigated the impact of using different initial cell densities of L. fermentum NG16 on its extracellular GABA production. Initial cell densities in MRS broth ranged from 5×105 to 5×107 CFU mL−1, while other conditions were kept constant, including MSG of 1% (w/v), temperature of 37 °C, initial pH of 6.2 and fermentation time of 24 h. An initial cell density of 5×106 CFU mL–1 yielded the highest GABA content in the spent culture medium, i.e. 16.30 ± 0.11 mM (Fig. 2). The lower GABA yields obtained at cell density of 5×105 CFU mL−1 and 106 CFU mL–1 likely resulted from the lower number of cells present, which might even had to adapt to a nutrient-rich environment, resulting in a delayed GABA peak yield (Thuy et al., 2021). Higher cell densities, in contrast, may provoke stress (Bunch, 1994), which leads to a decrease in GABA production. In comparison, Levilactobacillus namurensis NH2 and Pediococcus pentosaceus HN8 at a cell density of 106 CFU g–1 in a Thai fermented pork sausage produced a maximum GABA amount of 4.501 mg kg–1, which was higher than those at cell densities of 107 and 108 CFU g–1 (Ratanaburee et al., 2013).

Fig. 2.
Fig. 2.

GABA production by L. fermentum NG16 with different initial cell densities. Bars with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

3.3.2 Monosodium glutamate concentration

In many microorganisms including LAB, l-glutamate is converted to GABA via a decarboxylation reaction catalysed by GAD. As most LAB are unable to synthesise enough l-glutamic acid for GABA production (Cui et al., 2020), we supplemented various concentrations of monosodium glutamate (MSG) to the culture medium of L. fermentum NG16. The results showed that with an increase in MSG concentration from 0 to 2%, the yield of GABA proportionally increased as well (Fig. 3). This suggested that the increase in MSG concentration stimulated the production of GABA via the GABA shunt pathway (Feehily et al., 2013). The GABA content reached a maximum (18.13 ± 0.12 mM) at an MSG concentration of 2% (w/v). Various microorganisms have different optimal concentrations of MSG. For example, L. brevis CRL 1942 produces the highest amount of GABA at the optimal MSG content of ∼4.6% (w/v) (Villegas et al., 2016), while the optimal glutamate concentration for GABA production by Lacticaseibacillus paracasei NFRI 7415 is 8.46% (w/v) (Komatsuzaki et al., 2005).

Fig. 3.
Fig. 3.

GABA production by L. fermentum NG16 with different monosodium glutamate concentrations. Bars with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

3.3.3 Initial pH

The pH of the culture medium is a key parameter affecting GABA production by LAB as it affects not only bacterial growth but also the activity of the GAD system (Cui et al., 2020). The C-terminal region of GAD appeared associated with the enzyme's pH dependency (Yu et al., 2012). We, therefore, investigated the effect of initial pH on GABA synthesis by L. fermentum NG16. The results demonstrated that the GABA content in spent culture medium increased significantly with an increase in initial pH from 5 to 7 (Fig. 4). The highest GABA yield of 19.88 ± 0.33 mM was obtained at initial pH 7. At initial pH 8, GABA production decreased to 16.79 ± 0.18 mM. This reduction may be due to the inhibition of microbiological growth in the alkaline medium. It should be noted that the production of lactic acid during the fermentation process will cause a decrease in pH of the culture medium, which will affect both growth and activity of the GAD system. Thus, it was possible that strain L. fermentum NG16 had optimal growth or optimal GAD activity at initial pH 7 given that highest GABA yield was obtained at this initial pH value. In comparison, Komatsuzaki et al. (2005) reported that an initial pH of 5 was optimal for GABA production by L. paracasei NFRI 7415, while L. brevis GABA100 produced a maximum amount of GABA at initial pH 3.5 in the fermentation of black raspberry juice (Kim et al., 2009).

Fig. 4.
Fig. 4.

GABA production by L. fermentum NG16 at different initial culture medium pH values. Bars with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

3.3.4 Culture temperature

Together with culture pH, fermentation temperature is also a key factor affecting GABA production by LAB (Cui et al., 2020). In the present study, L. fermentum NG16 was inoculated into MSR broth at various culture temperatures, while initial cell density, MSG concentration, and initial pH were kept at 5×106 CFU mL–1, 2% (w/v), and 7, respectively. The GABA content in spent culture medium was quantified after 24 h of fermentation. The concentration of GABA increased markedly from 30 to 35 °C, reaching a peak of 21.29 ± 0.59 mM, but decreased gradually with further increase in incubation temperature (Fig. 5). The temperature may affect GABA production by acting on cell physiology or GAD activity. In this study, the temperature above 35 °C may have negative effect on cell growth, resulting in a reduction of GABA accumulation in the spent culture medium. Besides, incubation temperature may also affect GAD system in L. fermentum NG16, which needs to be further evaluated as the effect of temperature on GAD activity varies with LAB strains. For example, Shin et al. (2014) demonstrated that optimal temperature for the activity of GAD in L. plantarum ATCC 14917 was 40 °C, while Liu et al. (2021) documented that GAD purified from L. brevis F109-MD3 had an optimal temperature for its activity at 65 °C. In fact, different strains even of the same species produce maximum amount of GABA at different temperatures. For instance, the L. brevis strain GABA 100 produced a higher amount of GABA at a fermentation temperature of 30 °C compared to 37 or 25 °C (Kim et al., 2009), while the optimal temperature for GABA synthesis by L. brevis CRL 1942 was 37 °C (Villegas et al., 2016). In the present study, the highest GABA yield was obtained at a culture temperature of 35 °C, thus, this temperature was used for further experiments.

Fig. 5.
Fig. 5.

GABA production by L. fermentum NG16 at different culture temperatures. Bars with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

3.3.5 Time course study of pH, cell growth, and GABA production by L. fermentum NG16

Previously reported data showed that GABA accumulation in culture media is a function of fermentation time (Villegas et al., 2016; Thuy et al., 2021). Therefore, the effect of time on GABA yield as well as medium pH and cell growth of L. fermentum NG16 was investigated under optimal conditions of initial cell density, MSG concentration, initial pH, and fermentation temperature as determined above (Fig. 6). The results showed a concurrent increase in cell density and GABA content, which corresponded with a decrease in pH during the first 24 h. The pH decrease likely reflected lactic acid production by L. fermentum NG16. During the first 24 h of fermentation the pH value dropped sharply from 7 to around 5 and then remained stable until the end of the experiment at day 5 (Fig. 6A). The cell density increased sharply from around 7 to over 9 log CFU mL−1 during the first 24 h of fermentation. It then slowly increased further to reach a maximum of 9.334 ± 0.013 log CFU mL−1 after 72 h of fermentation after which it started to decline. The reduction in cell density after 72 h of fermentation (Fig. 6B) might be caused by nutrient depletion as well as autolysis of dead cells. Finally, during the first 24 h of fermentation, the GABA content increased proportionally with the increase in cell density and a decrease in pH, suggesting that GABA production occurred concurrently with lactic acid fermentation. In addition, there was a correspondence between GABA yield and cell density from 0 to 48 h of fermentation and a maximum level GABA concentration of 25.52 ± 0.41 mM was reached at 48 h of fermentation. After this 48 h period, GABA in the spent culture medium might be absorbed into the cells and degraded by GABA aminotransferase (Feehily et al., 2013) leading to a decrease in GABA yield (Fig. 6C).

Fig. 6.
Fig. 6.

Change of pH value (A), cell growth (B), and GABA concentration (C) during fermentation with L. fermentum NG16. Means with different letters differ significantly at P < 0.05

Citation: Acta Alimentaria 51, 2; 10.1556/066.2022.00065

4 Conclusions

Among 60 LAB isolates obtained from tuna gut samples, 7 were capable of GABA production. L. fermentum strain NG16 yielded the highest concentration of GABA in MRS broth supplemented with 1% (w/v) MSG, and its production of GABA was subsequently thoroughly characterised. The optimal batch culture conditions for GABA production by this strain were an initial cell density of 5×106 CFU mL−1, an MSG concentration of 2% (w/v), an initial pH of 7, a fermentation temperature of 35 °C, and an incubation time of 48 h. Under these optimal conditions, a maximum GABA level of 25.52 ± 0.41 mM in spent culture medium was obtained. The results of the present study provided a basis for the development and production of functional foods containing a high level of GABA.

Acknowledgment

We thank Margo Cnockaert (Laboratory of Microbiology, Ghent University, Belgium) for help with the identification of LAB isolates.

References

  • Bunch, A.W. (1994). High cell density growth of micro-organisms. Biotechnology and Genetic Engineering Reviews, 12(1): 535561.

  • Cui, Y. , Miao, K. , Niyaphorn, S. , and Qu, X. (2020). Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. International Journal of Molecular Sciences, 21(3): 995. 21 pages.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Diana, M. , Quílez, J. , and Rafecas, M. (2014). Gamma-aminobutyric acid as a bioactive compound in foods: a review. Journal of Functional Foods, 10: 407420.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Feehily, C. , O’Byrne, C.P. , and Karatzas, K.A.G. (2013). Functional γ-aminobutyrate shunt in Listeria monocytogenes: role in acid tolerance and succinate biosynthesis. Applied and Environmental Microbiology, 79(1): 7480.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Han, M. , Liao, W.-Y. , Wu, S.-M. , Gong, X. , and Bai, C. (2020). Use of Streptococcus thermophilus for the in situ production of γ-aminobutyric acid-enriched fermented milk. Journal of Dairy Science, 103(1): 98105.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kim, J.Y. , Lee, M.Y. , Ji, G.E. , Lee, Y.S. , and Hwang, K.T. (2009). Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. International Journal of Food Microbiology, 130(1): 1216.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Komatsuzaki, N. , Shima, J. , Kawamoto, S. , Momose, H. , and Kimura, T. (2005). Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiology, 22(6): 497504.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lappa, I.K. , Gantzias, C. , Manolopoulou, E. , De Brandt, E. , Aerts, M. , Vandamme, P. , Tsakalidou, E. , and Georgalaki, M. (2021). MALDI-TOF MS insight into the biodiversity of Staka, the artisanal Cretan soured cream. International Dairy Journal, 116: 104969.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Laroute, V. , Yasaro, C. , Narin, W. , Mazzoli, R. , Pessione, E. , Cocaign-Bousquet, M. , and Loubière, P. (2016). GABA Production in Lactococcus lactis is enhanced by arginine and co-addition of malate. Frontiers in Microbiology, 7: 1050.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Liu, W. , Li, H. , Liu, L. , Ko, K. , and Kim, I. (2021). Screening of gamma-aminobutyric acid-producing lactic acid bacteria and the characteristic of glutamate decarboxylase from Levilactobacillus brevis F109-MD3 isolated from kimchi. Journal of Applied Microbiology, 132(3): 19671977.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ratanaburee, A. , Kantachote, D. , Charernjiratrakul, W. , and Sukhoom, A. (2013). Enhancement of γ-aminobutyric acid (GABA) in Nham (Thai fermented pork sausage) using starter cultures of Lactobacillus namurensis NH2 and Pediococcus pentosaceus HN8. International Journal of Food Microbiology, 167(2). 170176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sanchart, C. , Rattanaporn, O. , Haltrich, D. , Phukpattaranont, P. , and Maneerat, S. (2017). Enhancement of gamma-aminobutyric acid (GABA) levels using an autochthonous Lactobacillus futsaii CS3 as starter culture in Thai fermented shrimp (Kung-Som). World Journal of Microbiology and Biotechnology, 33(8): 152.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Shin, S.-M. , Kim, H. , Joo, Y. , Lee, S.-J. , Lee, Y.-J. , Lee, S.J. , and Lee, D.-W. (2014). Characterization of glutamate decarboxylase from Lactobacillus plantarum and its C-terminal function for the pH dependence of activity. Journal of Agricultural and Food Chemistry, 62(50): 1218612193.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Somkuti, G.A. , Renye, J.A. , and Steinberg, D.H. (2012). Molecular analysis of the glutamate decarboxylase locus in Streptococcus thermophilus ST110. Journal of Industrial Microbiology and Biotechnology, 39(7): 957963.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thuy, D.T.B. , Nguyen, A.T. , Khoo, K.S. , Chew, K.W. , Cnockaert, M. , Vandamme, P. , Ho, Y.C. , Huy, N D. , Cocoletzi, H.H. , and Show, P.L. (2021). Optimization of culture conditions for gamma-aminobutyric acid production by newly identified Pediococcus pentosaceus MN12 isolated from ‘mam nem’, a fermented fish sauce. Bioengineered, 12(1): 5462.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Villegas, J.M. , Brown, L. , Savoy de Giori, G. , and Hebert, E.M. (2016). Optimization of batch culture conditions for GABA production by Lactobacillus brevis CRL 1942, isolated from quinoa sourdough. LWT - Food Science and Technology, 67: 2226.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wieme, A.D. , Spitaels, F. , Aerts, M. , De Bruyne, K. , Van Landschoot, A. , and Vandamme, P. (2014). Identification of beer-spoilage bacteria using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. International Journal of Food Microbiology, 185: 4150.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yang, T. , Rao, Z. , Kimani, B.G. , Xu, M. , Zhang, X. , and Yang, S.T. (2015). Two-step production of gamma-aminobutyric acid from cassava powder using Corynebacterium glutamicum and Lactobacillus plantarum. Journal of Industrial Microbiology and Biotechnology, 42(8): 11571165.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yu, K. , Lin, L. , Hu, S. , Huang, J. , and Mei, L. (2012). C-terminal truncation of glutamate decarboxylase from Lactobacillus brevis CGMCC 1306 extends its activity toward near-neutral pH. Enzyme and Microbial Technology, 50(4–5): 263269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yunes, R.A. , Poluektova, E.U. , Dyachkova, M.S. , Klimina, K.M. , Kovtun, A.S. , Averina, O.V. , Orlova, V.S. , and Danilenko, V.N. (2016). GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe, 42: 197204.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bunch, A.W. (1994). High cell density growth of micro-organisms. Biotechnology and Genetic Engineering Reviews, 12(1): 535561.

  • Cui, Y. , Miao, K. , Niyaphorn, S. , and Qu, X. (2020). Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. International Journal of Molecular Sciences, 21(3): 995. 21 pages.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Diana, M. , Quílez, J. , and Rafecas, M. (2014). Gamma-aminobutyric acid as a bioactive compound in foods: a review. Journal of Functional Foods, 10: 407420.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Feehily, C. , O’Byrne, C.P. , and Karatzas, K.A.G. (2013). Functional γ-aminobutyrate shunt in Listeria monocytogenes: role in acid tolerance and succinate biosynthesis. Applied and Environmental Microbiology, 79(1): 7480.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Han, M. , Liao, W.-Y. , Wu, S.-M. , Gong, X. , and Bai, C. (2020). Use of Streptococcus thermophilus for the in situ production of γ-aminobutyric acid-enriched fermented milk. Journal of Dairy Science, 103(1): 98105.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kim, J.Y. , Lee, M.Y. , Ji, G.E. , Lee, Y.S. , and Hwang, K.T. (2009). Production of γ-aminobutyric acid in black raspberry juice during fermentation by Lactobacillus brevis GABA100. International Journal of Food Microbiology, 130(1): 1216.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Komatsuzaki, N. , Shima, J. , Kawamoto, S. , Momose, H. , and Kimura, T. (2005). Production of γ-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiology, 22(6): 497504.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lappa, I.K. , Gantzias, C. , Manolopoulou, E. , De Brandt, E. , Aerts, M. , Vandamme, P. , Tsakalidou, E. , and Georgalaki, M. (2021). MALDI-TOF MS insight into the biodiversity of Staka, the artisanal Cretan soured cream. International Dairy Journal, 116: 104969.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Laroute, V. , Yasaro, C. , Narin, W. , Mazzoli, R. , Pessione, E. , Cocaign-Bousquet, M. , and Loubière, P. (2016). GABA Production in Lactococcus lactis is enhanced by arginine and co-addition of malate. Frontiers in Microbiology, 7: 1050.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Liu, W. , Li, H. , Liu, L. , Ko, K. , and Kim, I. (2021). Screening of gamma-aminobutyric acid-producing lactic acid bacteria and the characteristic of glutamate decarboxylase from Levilactobacillus brevis F109-MD3 isolated from kimchi. Journal of Applied Microbiology, 132(3): 19671977.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ratanaburee, A. , Kantachote, D. , Charernjiratrakul, W. , and Sukhoom, A. (2013). Enhancement of γ-aminobutyric acid (GABA) in Nham (Thai fermented pork sausage) using starter cultures of Lactobacillus namurensis NH2 and Pediococcus pentosaceus HN8. International Journal of Food Microbiology, 167(2). 170176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sanchart, C. , Rattanaporn, O. , Haltrich, D. , Phukpattaranont, P. , and Maneerat, S. (2017). Enhancement of gamma-aminobutyric acid (GABA) levels using an autochthonous Lactobacillus futsaii CS3 as starter culture in Thai fermented shrimp (Kung-Som). World Journal of Microbiology and Biotechnology, 33(8): 152.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Shin, S.-M. , Kim, H. , Joo, Y. , Lee, S.-J. , Lee, Y.-J. , Lee, S.J. , and Lee, D.-W. (2014). Characterization of glutamate decarboxylase from Lactobacillus plantarum and its C-terminal function for the pH dependence of activity. Journal of Agricultural and Food Chemistry, 62(50): 1218612193.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Somkuti, G.A. , Renye, J.A. , and Steinberg, D.H. (2012). Molecular analysis of the glutamate decarboxylase locus in Streptococcus thermophilus ST110. Journal of Industrial Microbiology and Biotechnology, 39(7): 957963.

    • Crossref
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    • Export Citation
  • Thuy, D.T.B. , Nguyen, A.T. , Khoo, K.S. , Chew, K.W. , Cnockaert, M. , Vandamme, P. , Ho, Y.C. , Huy, N D. , Cocoletzi, H.H. , and Show, P.L. (2021). Optimization of culture conditions for gamma-aminobutyric acid production by newly identified Pediococcus pentosaceus MN12 isolated from ‘mam nem’, a fermented fish sauce. Bioengineered, 12(1): 5462.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Villegas, J.M. , Brown, L. , Savoy de Giori, G. , and Hebert, E.M. (2016). Optimization of batch culture conditions for GABA production by Lactobacillus brevis CRL 1942, isolated from quinoa sourdough. LWT - Food Science and Technology, 67: 2226.

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    • Export Citation
  • Wieme, A.D. , Spitaels, F. , Aerts, M. , De Bruyne, K. , Van Landschoot, A. , and Vandamme, P. (2014). Identification of beer-spoilage bacteria using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. International Journal of Food Microbiology, 185: 4150.

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    • Export Citation
  • Yang, T. , Rao, Z. , Kimani, B.G. , Xu, M. , Zhang, X. , and Yang, S.T. (2015). Two-step production of gamma-aminobutyric acid from cassava powder using Corynebacterium glutamicum and Lactobacillus plantarum. Journal of Industrial Microbiology and Biotechnology, 42(8): 11571165.

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    • Export Citation
  • Yu, K. , Lin, L. , Hu, S. , Huang, J. , and Mei, L. (2012). C-terminal truncation of glutamate decarboxylase from Lactobacillus brevis CGMCC 1306 extends its activity toward near-neutral pH. Enzyme and Microbial Technology, 50(4–5): 263269.

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  • Yunes, R.A. , Poluektova, E.U. , Dyachkova, M.S. , Klimina, K.M. , Kovtun, A.S. , Averina, O.V. , Orlova, V.S. , and Danilenko, V.N. (2016). GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe, 42: 197204.

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    • Export Citation

 

The author instruction is available in PDF.
Please, download the file from HERE.

Senior editors

Editor(s)-in-Chief: András Salgó

Co-ordinating Editor(s) Marianna Tóth-Markus

Co-editor(s): A. Halász

       Editorial Board

  • L. Abrankó (Szent István University, Gödöllő, Hungary)
  • D. Bánáti (University of Szeged, Szeged, Hungary)
  • J. Baranyi (Institute of Food Research, Norwich, UK)
  • I. Bata-Vidács (Agro-Environmental Research Institute, National Agricultural Research and Innovation Centre, Budapest, Hungary)
  • J. Beczner (Food Science Research Institute, National Agricultural Research and Innovation Centre, Budapest, Hungary)
  • F. Békés (FBFD PTY LTD, Sydney, NSW Australia)
  • Gy. Biró (National Institute for Food and Nutrition Science, Budapest, Hungary)
  • A. Blázovics (Semmelweis University, Budapest, Hungary)
  • F. Capozzi (University of Bologna, Bologna, Italy)
  • M. Carcea (Research Centre for Food and Nutrition, Council for Agricultural Research and Economics Rome, Italy)
  • Zs. Cserhalmi (Food Science Research Institute, National Agricultural Research and Innovation Centre, Budapest, Hungary)
  • M. Dalla Rosa (University of Bologna, Bologna, Italy)
  • I. Dalmadi (Szent István University, Budapest, Hungary)
  • K. Demnerova (University of Chemistry and Technology, Prague, Czech Republic)
  • M. Dobozi King (Texas A&M University, Texas, USA)
  • Muying Du (Southwest University in Chongqing, Chongqing, China)
  • S. N. El (Ege University, Izmir, Turkey)
  • S. B. Engelsen (University of Copenhagen, Copenhagen, Denmark)
  • E. Gelencsér (Food Science Research Institute, National Agricultural Research and Innovation Centre, Budapest, Hungary)
  • V. M. Gómez-López (Universidad Católica San Antonio de Murcia, Murcia, Spain)
  • J. Hardi (University of Osijek, Osijek, Croatia)
  • K. Héberger (Research Centre for Natural Sciences, ELKH, Budapest, Hungary)
  • N. Ilić (University of Novi Sad, Novi Sad, Serbia)
  • D. Knorr (Technische Universität Berlin, Berlin, Germany)
  • H. Köksel (Hacettepe University, Ankara, Turkey)
  • K. Liburdi (Tuscia University, Viterbo, Italy)
  • M. Lindhauer (Max Rubner Institute, Detmold, Germany)
  • M.-T. Liong (Universiti Sains Malaysia, Penang, Malaysia)
  • M. Manley (Stellenbosch University, Stellenbosch, South Africa)
  • M. Mézes (Szent István University, Gödöllő, Hungary)
  • Á. Németh (Budapest University of Technology and Economics, Budapest, Hungary)
  • P. Ng (Michigan State University,  Michigan, USA)
  • Q. D. Nguyen (Szent István University, Budapest, Hungary)
  • L. Nyström (ETH Zürich, Switzerland)
  • L. Perez (University of Cordoba, Cordoba, Spain)
  • V. Piironen (University of Helsinki, Finland)
  • A. Pino (University of Catania, Catania, Italy)
  • M. Rychtera (University of Chemistry and Technology, Prague, Czech Republic)
  • K. Scherf (Technical University, Munich, Germany)
  • R. Schönlechner (University of Natural Resources and Life Sciences, Vienna, Austria)
  • A. Sharma (Department of Atomic Energy, Delhi, India)
  • A. Szarka (Budapest University of Technology and Economics, Budapest, Hungary)
  • M. Szeitzné Szabó (National Food Chain Safety Office, Budapest, Hungary)
  • S. Tömösközi (Budapest University of Technology and Economics, Budapest, Hungary)
  • L. Varga (University of West Hungary, Mosonmagyaróvár, Hungary)
  • R. Venskutonis (Kaunas University of Technology, Kaunas, Lithuania)
  • B. Wróblewska (Institute of Animal Reproduction and Food Research, Polish Academy of Sciences Olsztyn, Poland)

 

Acta Alimentaria
E-mail: Acta.Alimentaria@uni-mate.hu

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2021  
Web of Science  
Total Cites
WoS
856
Journal Impact Factor 1,000
Rank by Impact Factor Food Science & Technology 130/143
Nutrition & Dietetics 81/90
Impact Factor
without
Journal Self Cites
0,941
5 Year
Impact Factor
1,039
Journal Citation Indicator 0,19
Rank by Journal Citation Indicator Food Science & Technology 143/164
Nutrition & Dietetics 92/109
Scimago  
Scimago
H-index
30
Scimago
Journal Rank
0,235
Scimago Quartile Score

Food Science (Q3)

Scopus  
Scopus
Cite Score
1,4
Scopus
CIte Score Rank
Food Sciences 222/338 (Q3)
Scopus
SNIP
0,387

 

2020
 
Total Cites
768
WoS
Journal
Impact Factor
0,650
Rank by
Nutrition & Dietetics 79/89 (Q4)
Impact Factor
Food Science & Technology 130/144 (Q4)
Impact Factor
0,575
without
Journal Self Cites
5 Year
0,899
Impact Factor
Journal
0,17
Citation Indicator
 
Rank by Journal
Nutrition & Dietetics 88/103 (Q4)
Citation Indicator
Food Science & Technology 142/160 (Q4)
Citable
59
Items
Total
58
Articles
Total
1
Reviews
Scimago
28
H-index
Scimago
0,237
Journal Rank
Scimago
Food Science Q3
Quartile Score
 
Scopus
248/238=1,0
Scite Score
 
Scopus
Food Science 216/310 (Q3)
Scite Score Rank
 
Scopus
0,349
SNIP
 
Days from
100
submission
 
to acceptance
 
Days from
143
acceptance
 
to publication
 
Acceptance
16%
Rate
2019  
Total Cites
WoS
522
Impact Factor 0,458
Impact Factor
without
Journal Self Cites
0,433
5 Year
Impact Factor
0,503
Immediacy
Index
0,100
Citable
Items
60
Total
Articles
59
Total
Reviews
1
Cited
Half-Life
7,8
Citing
Half-Life
9,8
Eigenfactor
Score
0,00034
Article Influence
Score
0,077
% Articles
in
Citable Items
98,33
Normalized
Eigenfactor
0,04267
Average
IF
Percentile
7,429
Scimago
H-index
27
Scimago
Journal Rank
0,212
Scopus
Scite Score
220/247=0,9
Scopus
Scite Score Rank
Food Science 215/299 (Q3)
Scopus
SNIP
0,275
Acceptance
Rate
15%

 

Acta Alimentaria
Publication Model Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article
Printed Color Illustrations 40 EUR (or 10 000 HUF) + VAT / piece
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription fee 2022 Online subsscription: 754 EUR / 944 USD
Print + online subscription: 872 EUR / 1090 USD
Subscription fee 2023 Online subsscription: 776 EUR / 944 USD
Print + online subscription: 896 EUR / 1090 USD
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Purchase per Title Individual articles are sold on the displayed price.

Acta Alimentaria
Language English
Size B5
Year of
Foundation
1972
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia    
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0139-3006 (Print)
ISSN 1588-2535 (Online)

 

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Jul 2022 0 11 12