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
Highlights
► One strain, Lactobacillus brevis FPA 3709, from 126 lactic acid bacteria isolated from fish intestines was chosen for GABA production. ► FPA3709 produces a very high amount of GABA in formulated black soybean milk at 37 °C for 48 h. ► The 48-h fermented product has similar antidepressant activity as fluoxetine but without side effects caused by fluoxetine.
Introduction
Depression is a widespread incapacitating psychiatric ailment ranked by the World Health Organization (WHO) as one of the most burdensome diseases of society [1], [2]. Despite the prevalence and severe effects of this disease, the efficacy of the currently available antidepressants is often inconsistent, and many exert undesirable side effects.
Gamma-aminobutyric acid (GABA), a 4-carbon non-proteinaceous amino acid found ubiquitously in nature, has various physiological functions, such as hypotensive [3], hypoglycemic [4], and anticancer activities [5]. Several studies have recently demonstrated that the dysfunction of GABAergic neurons, which are responsible for GABA production, is involved in depression [6], [7], [8], anxiety [9], and Alzheimer's disease [10]. Depressed patients show significantly reduced activity of GABAergic neurons in the prefrontal or occipital cortex, leading to greatly decreased GABA levels in these 2 areas and in the plasma and cerebrospinal fluid of depressed patients [11], [12], [13]. Therefore, searching for GABA-rich foods has become a relevant topic in the field of functional foods. Researchers have developed numerous GABA-rich products, such as GABA tea [14], [15], germinated crops, including brown rice [16], barley [17], and wheat [18], red mold rice [19], [20], and various fermented foods produced by GABA-producing lactic acid bacteria (LAB) [21], [22], [23].
Researchers have reported GABA-producing LAB strains from various sources, including Lactobacillus lactis subsp. lactis from kimchi [24], Lactobacillus brevis from alcohol distillery lees [25], Lactobacillus paracasei from fermented fish [26], and L. delbrueckii subsp. bulgaricus from cheese [27]. Researchers have also sequenced their genes for glutamic acid decarboxylase (GAD), which catalyze the decarboxylation of l-glutamate for GABA synthesis.
The LAB currently used in the food industry are mainly isolated from human feces [28], plants [29], and various fermented products, such as kimchi [23], [30], cheese [27], tempeh [31], and sausage [32]. Only a few LAB have been isolated from fish intestines [33]. The aims of this study are as follows: to isolate LAB from fish intestines and select the highest GABA-producing LAB isolate; to establish the ideal bean milk among 3 tested samples of black soybean, soybean, and red bean milk as the basal substrate; to optimize the culture conditions to increase the concentration of GABA produced during fermentation by LAB isolate and to test, using a forced swimming test (FST), the antidepressant effect of fermented bean milk after orally feeding it to Sprague-Dawley (SD) rats.
Section snippets
LAB isolation from fish intestines
Fifteen fish samples (Priacanthus macracanthus, Psenopsis anomala, Pseudosciaena polyactis, Lateolabrax japonicas, Cololabis saira, Calotomus carolinus, Scomber australasicus, Kuhlia rupestris, Leopard coralgrouper, Taius tumifrons, Priacanthus macracanthusthu, Pampus agrenteus, Branchiostegus japonicas, Epinephelus malabaricus, and Polydactylus plebeius) were purchased from local fish markets in Keelung, Taiwan. The fish were kept in an icebox and immediately transferred to the laboratory.
LAB isolation from fish intestines and screening for isolates with GABA production
The experiments in this study involved analyzing 126 LAB isolates from 15 fish samples. All of these isolates were confirmed to be Gram-positive, catalase-negative, and oxidase-negative, and produce sufficient acid (data not shown), which are the basic characteristics of LAB.
The GABA production of 126 LAB isolates in MRS with 5% MSG was screened by TLC. Fig. 1 shows the TLC profiles of certain representatives. The isolates with a visible band of GABA are FPP3713, FPA3709, FKR3737, FKR3739, and
Discussion
Although GAD is widely found in LAB [41], the GABA-producing capability of LAB may vary between strains. Previous studies have isolated GABA-producing LAB from cheese and dairy products [27], [41], wine spent [25], and fermented kimchi products [23], [36], [42]. This is the first study to report on the isolation of GABA-producing LAB from fish intestines for application in food fermentation.
Cooking treatment by heating soaked bean grains in water at 100 °C for 50 min may soften the bean, which
Conclusion
Cooked black soybean milk was an ideal basal substrate for GABA production by L. brevis FPA 3709 isolated from fish intestine. FPA3709 produced a high amount of GABA (5.42 ± 0.39 mg/mL) in cooked black soybean milk with 1% MSG, 1% brown sugar, and 0.1% peptone without pH control after incubation at 37 °C for 48 h. This 48-h fermented black soybean milk had an antidepressant effect similar to that of fluoxetine, but without the side effects of lost appetite and decreased weight. The underlying
Acknowledgments
The authors gratefully acknowledge the financial support of the National Science Council of Taiwan, R.O.C. (NSC98-2313-B-019-010-MY3) and the Center of Marine Bioenvironment and Biotechnology, National Taiwan Ocean University (NTOU-RD-AA-2012-102011).
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