Production of Gamma-Aminobutyric Acid by L. plantarum

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Production of Gamma-Aminobutyric Acid by L. plantarum

This entry is adapted from the peer-reviewed paper 10.3390/cimb46010015

Given the important role of gamma-aminobutyric acid (GABA) in human health, scientists have paid great attention to the enrichment of this chemical compound in food using various methods, including microbial fermentation. Moreover, GABA or GABA-rich products have been successfully commercialized as food additives or functional dietary supplements. Several microorganisms can produce GABA, including bacteria, fungi, and yeasts. Among GABA-producing microorganisms, lactic acid bacteria (LAB) are commonly used in the production of many fermented foods. Lactiplantibacillus plantarum (formerly Lactobacillus plantarum) is a LAB species that has a long history of natural occurrence and safe use in a wide variety of fermented foods and beverages. Within this species, some strains possess not only good pro-technological properties but also the ability to produce various bioactive compounds, including GABA.

Lactobacillus plantarum functional food L-glutamate decarboxylase lactic acid bacteria

1. Introduction

The production of GABA varies among various LAB strains and is affected by several factors such as pH, fermentation temperature, fermentation time, L-glutamic acid concentration, media additives, and carbon and nitrogen sources ^[1]^[2]^[3]^[4]. The optimization of these parameters could maximize the amount of GABA contained in some LAB-fermented foods ^[1]^[5].

In recent years, many researchers have studied L. plantarum, in particular, for its ability to synthesize GABA in different substrates and growing conditions.

The most commonly used culture medium is MRS (de Man, Rogosa and Sharp), a standard substrate designed to promote LAB growth ^[6]. Monosodium glutamate (MSG), as a source of L-glutamine, is usually supplemented directly into MRS to enhance GABA synthesis from L. plantarum strains ^[7].

However, the optimal concentration of MSG depends on the bacterial strain. For example, Yogeswara et al. investigated the GABA production from L. plantarum FNCC 260 strain using a wide range of MSG concentrations. The results showed a maximum GABA production (1226 mg/L) by adding 100 mM of MSG to the MRS medium and then incubating at 37 °C for 108 h ^[8].

In another study, after 18 h at 34 °C, L. plantarum K74 produced 134.52 μg/mL of GABA in MRS broth containing 1% MSG, 212.27 μg/mL of GABA in MRS broth containing 2% MSG, and 234.63 μg/mL of GABA in MRS broth containing 3% MSG ^[9].

Gomaa et al. examined the effect of MSG and PLP on GABA production from L. brevis and L. plantarum strains, isolated from Egyptian dairy products. The culture medium used was the following composition: 50 g/L glucose; 25 g/L soya peptone; 0.01 g/L MnSO₄C₄H₂O and 2 mL Tween 80. The results of the aforementioned study show that the amount of extracellular GABA produced is proportional to the amounts of MSG and PLP added. Co-culture of L. brevis and L. plantarum produced the highest amount of GABA, 160.57 mM and 224.69 mM, in the presence of 750 M MSG and 200 μM PLP, respectively ^[10].

Park et al. have obtained high amounts of GABA (19.8 g/L) at 30 °C from L. plantarum EJ2014 using the following culture medium: 100 g/L Yeast extract, 10 g/L dextrose, and 22.5 g/L (w/v) MSG ^[4].

In a study conducted by Shan et al. L. plantarum NDC75017 produced 3.2 g/kg of GABA, at 30 °C for 48 h, in skimmed milk with 80 mM MSG and 18 μM PLP ^[11].

As evidenced in all the studies mentioned above, the amount of monosodium glutamate initially available is an important factor in the production of GABA ^[12].

In fact, as also confirmed in other studies cited below, an initial excessive concentration of MSG may inhibit cell growth or inhibit GABA production due to osmotic stress, while a low concentration of MSG may not meet the requirements of high GABA production ^[13]. As far as the incubation time is concerned, the amount of GABA after reaching the maximum amount after a certain period of time, tends to decrease subsequently. This effect may be caused by a lower availability of precursors (e.g., MSG) but also be linked to degradation, by GABA aminotransferase, of GABA to succinic semialdehyde, which is subsequently converted by succinic semialdehyde dehydrogenase for entry into TCA ^[14].

Temperature and pH have been reported as the main environmental factors that can modulate gad gene expression ^[15]. Therefore, adjusting pH and temperature during fermentation is a very effective way to increase microbial GABA production.

LAB employ a complex but efficient combination of different acid resistance systems ^[16].

Among the various types of tolerance mechanisms to the acidic environment, the GAD system is considered one of the most effective acid mitigation pathways.

In this system, intracellular protons are consumed through decarboxylation of glutamate in the cytoplasm ^[17].

Shin et al. showed that 40 °C and a pH of 4.5 were the best parameters for the expression of gadB gene encoding GAD from L. plantarum ATCC 14,917 in E. coli BL21 (DE3) ^[18].

Variation in pH enhances activation of the GAD pathway since it is considered one of the mechanisms that preserve cell homeostasis ^[19]. Wu et al. evaluated the performance of the GAD pathway in comparison with other acid resistance mechanisms and highlighted how the GAD system is an essential mechanism to maintain metabolic activity under intra- and extracellular acidity ^[20].

Therefore, the pH of the environment is crucial for the synthesis of GABA. However, it seems that this depends on the bacterial strain ^[18].

Zhang et al. tested how initial pH affects GABA production by L. plantarum BC114. The best concentration of GABA was detected at pH 5.5, obtaining double the amount of GABA yielded at pH 4.0 ^[21]. Similar results have been obtained in other studies ^[22]^[23]^[24].

Tajabadi et al. found that after 60 h L. plantarum Taj-Apis362 produces the highest amount of GABA (7.15 mM; 0.74 g/L) at 36 °C in modified MRS: 497.97 mM glutamate, pH 5.31 ^[22]. Tanamool et al. found that the highest GABA production (15.74 g/L) by L. plantarum L10-11 cultured in MRS with 4% MSG at 30 °C was obtained within 48 h, with a pH range of 5–6 ^[23].

Very recently, Cai et al. reported that L. plantarum FRT7 after 48 h produced approximately 1.2 g/L in MRS supplemented with 3% MSG and 2 mmol/L of PLP at 40° C with an initial pH of 7.0 ^[24].

In a recent study conducted by Kim J et al., the optimal conditions for efficient GABA production by L. plantarum FBT215 in modified MRS broth containing 50 mM MSG were investigated. Therefore, the optimal culture temperature for GABA production (103.67 μg/mL) was 37 °C and this efficiency was highest at pH 7.5 and 8.5 and decreased under acidic conditions ^[25].

Instead, Yogeswara et al. found that GABA production from L. plantarum FNCC 260 was greatly improved under acidic conditions (pH 3.8) in Pigeon pea (Cajanus cajan) milk fermentation ^[26]. This result is in line with a previous study by Yogeswara et al. where maximum GABA production from L. plantarum FNCC 260 in MRS was observed at pH 4.0 ^[8].

Regarding the temperature, Yang et al. reported that GAD functionality is directly related to an increase in temperature until it reaches an optimum, after which GAD activity decreases until thermal inactivation ^[27]. Another study with L. plantarum showed an increase in GAD activity up to 40 °C, achieving optimal GABA production at 35 °C ^[11].

2. GABA Production by L. plantarum in Fermented Foods

According to the available data, naturally occurring GABA in foods is usually low ^[2]^[28]; therefore, the food industry has shown great interest in GABA-enriched foods, through microbial fermentation.

Currently, L. plantarum is a LAB species commonly found in various fermented foods and beverages. Therefore, some food scientists have proposed strains of L. plantarum as starters in single culture or in co-culture with other microbial species to enrich GABA in some traditional or innovative fermented foods, particularly from plant-based sources.

In a recent study ^[26], it has been proposed a drink prepared from germinated pigeon pea (Cajanus cajan) and fermented using probiotic L. plantarum Dad-13, isolated from dadih, fermented buffalo milk ^[29]. C. cajan commonly known as pigeon pea, red gram or gungo pea is an important grain legume crop, particularly in rain-fed agricultural regions in the semi-arid tropics, including Asia, Africa and the Caribbean ^[30].

Additional nutrients such as MSG 1%, whey 4%, and sucrose 3% were added to pigeon pea extract and fermentation was carried out in a closed container at 30 °C for 48 h without shaking. Maximum GABA production (5.6 g/L) was obtained after 12 h of fermentation.

Wang et al. have shown that it is possible to increase the production of GABA in fermented lychee juice by L. plantarum HU-C2W ^[31]. Litchi (Litchi chinensis Sonn.) is a well-known tropical fruit originating from Asia ^[32]. After 40 h at 37 °C, a GABA content of 134 mg/100 mL was observed ^[31].

In various studies, L. plantarum DW12, isolated by Ratanaburee et al. from a fermented red seaweed, has been successfully used as probiotic and starter culture to produce fermented foods and beverages due to its safety aspects and ability to produce GABA ^[33]^[34]^[35]^[36].

The results obtained in ^[34] reported that L. plantarum DW12 produces 4 g/L GABA in red seaweed fermentation (red seaweed-cane sugar-potable water = 3:1:10, w/w/v) at 30 °C after 60 days. The red seaweed Gracilaria fisheri is commonly found along the coast of south-east Asian countries and used as a fresh vegetable and as a dried product ^[37].

In another study conducted by Hayisama-Ae et al., a novel functional beverage was produced from red seaweed Gracilaria fisheri (known as Pom Nang seaweed in Thailand), using L. plantarum DW12 as a starter culture ^[35]. Fermented red seaweed beverage was produced as follows: red seaweed, cane sugar and potable water in a ratio of 3:1:10 with an addition of 0.5% of MSG and an initial pH of 6.0. After 60 days the fermented red seaweed beverage (FSB) contained 1.28 g/L GABA.

A study conducted by Kantachote et al. aimed to add value to mature coconut water by using the probiotic L. plantarum DW12 for the production of GABA-enriched fermented beverages. Coconut water, with an initial pH of 5.0, was supplemented with 0.5% monosodium glutamate and 1% sugarcane and fermented from L. plantarum DW12. After 48 h, the fermented product contained 128 μg/mL of GABA ^[36].

Coconut (Cocos nucifera L.) is an important fruit tree found in tropical regions and its fruit can be made into a variety of foods and beverages ^[38].

Zarei et al. investigated the potential of GABA production by a L. plantarum strain in whey protein beverage ^[39], building on previous research, in which this strain, isolated from traditional doogh (yogurt, herbs and water) from west region of Iran, have shown a high concentration of GABA production (170.492 ppm) in MRS broth ^[40]. The best growing conditions that caused the highest GABA production were temperature 37 °C, pH 5.19, glutamic acid 250 mM, and time 72 h. The highest amount of GABA (195.5 ppm) after 30 days of storage was detected in whey protein drinks containing banana concentrate and stored at 25 °C.

L. plantarum NDC75017 (isolated from a traditional fermented dairy product from Inner Mongolia, China) was used as a starter for fermentation at 36°of Skim Milk and 80 mM L-MSG and 18 μM PLP. Under these conditions, GABA production was about 310 mg/100 g ^[11].

In a study conducted by Di Cagno et al., the use of L. plantarum DSM19463 (formerly L. plantarum C48) for the production of a functional grape-based beverage was evaluated ^[41]. The grape must, diluted with water, was enriched with yeast extract and 18.4 mM of L-glutamate and left to ferment at 30 °C. After 72 h L. plantarum DSM19463 synthesizes 4.83 mM of GABA ^[41].

In another study, the L. plantarum C48 has been used in sourdough fermentation ^[42].

The use of a blend of buckwheat, amaranth, chickpea and quinoa flours (ratio 1:1:5.3:1) subjected to sourdough fermentation by L. plantarum C48 allowed the manufacture of a bread enriched with GABA (504 mg/kg) ^[43]. The sourdough starter obtained with L. plantarum C48 had GABA concentrations of 12.65, 100.71 and 44.61 mg/kg for white, whole wheat and rye flours, respectively ^[43].

In another recent study, L. plantarum VL1 was used for the production of Nem Chua (traditionally Vietnamese fermented meat product). Fresh pork without fat was minced and mixed with 5% salt, 20% sugar, and 1% sodium glutamate. L. plantarum VL1, was added to the mixture and after 72 h of fermentation at 37 °C the meat mixture (pH 4.59) contained 1.1 mg/g of GABA ^[44].

In a study conducted by Nakatani et al. L. plantarum KB1253, isolated from Japanese pickles, is used in GABA-enriched tomato juice production ^[45]. This strain produces 41.0 mM GABA from 46.8 mM glutamate in tomato juice (pH 4.0, 20°Bx) incubated for 24 h at 35°.

In another study conducted by Rezaei et al., the GABA-producing strain L. plantarum IBRC (10817) was used in the production of a probiotic beverage made from black grapes. After 21 days, the fermented beverage had a concentration of 117.33 mg/L GABA ^[46].

L. plantarum K16 isolated from kimchi has been used to valorize some agri-food by-products ^[47], obtained from tomatoes, apples, oranges and green peppers. The agri-food by-products were enriched with 25 g/L of glucose, 12 g/L of yeast extract and 500 mM of MSG. Subsequently, the pH was adjusted to 5.5, and the media were inoculated with L. plantarum K16 and incubated at 34 °C for 96 h. L. plantarum K16 produced the following concentrations of GABA: 1166.81 mg/L, 1280.01 mg/L, 1626.52 mg/L and 1776.75 mg/L in apple, orange, green pepper and tomato by-products, respectively ^[48].

GABA is an important molecule naturally present in food matrices of plant and animal origin. However, plant-based foods contain a comparatively lower amount of GABA than animal-based foods ^[49]^[50].

Considering its potential health benefits, the studies mentioned above have shown that it is possible to increase the amount of GABA not only in some animal products but also in some fermented plant-based foods and beverages, improving their functional properties. In particular, it has been shown that through the use of L. plantarum as a single starter, it has been possible to produce fermented foods from legumes, cereals, fruit juices and some agri-food by-products containing high amounts of GABA.

Besides its use as a single culture, the use of L. plantarum in co-culture (co-fermentation or two-stage fermentation) with other microbial strains belonging to different species is gaining increasing interest.

In a study conducted by Hussin et al. ^[13], the effect of different carbohydrates was investigated on enhancing GABA production in yogurt cultured using a mixture of UPMC90 and UPMC91, self-cloned LAB strains (L. plantarum Taj-Apis362, previously isolated from the stomach of honeybee Apis dorsata and engineered by Tajabadi et al. ^[22]^[51]). Glucose induced more GABA production (58.56 mg/100 g) compared to inuline, FOS e GOS as prebiotics (34.19–40.51 mg/100 g), and the control sample with added PLP (48.01 mg/100 g) ^[13].

In other similar study, conducted by Hussin et al., self-cloned and expressed L. plantarum Taj-Apis362 recombinant cells, UPMC90 and UPMC91 were used to improve the GABA production in yogurt. Fermentation of skimmed milk added with glutamate (11.5 mM) after 7.25 h at 39.0 °C produced GABA-rich yogurt (29.96 mg/100 g) ^[52].

While many studies reported the use of single-strain LAB to generate GABA, only a few reported the production of GABA by co-culturing different bacterial strains ^[53].

In a study carried out by Lim et al., the co-fermentation of turmeric (Curcuma longa)/roasted soybean meal mixture, containing 5% MSG, was optimized to fortify it with bioactive compounds including GABA ^[54]. Bacillus subtilis HA was used for the first fermentation and L. plantarum K154 isolated from fermented kimchi was used for the second fermentation. The results showed that the amount of GABA increased from 0.01% before fermentation to 1.78% after the second fermentation ^[55].

In a further study, a two-step fermentation of pumpkin (Cucurbita moschata) was performed using B. subtilis HA and L. plantarum EJ2014, with the aim of producing a novel food ingredient enriched with GABA ^[56]. Bacillus subtilis HA (KCCM 10775P) strain was isolated from cheonggukjang (traditional Korean fermented soybean) while L. plantarum EJ2014 (KCCM 11545P) was isolated from rice bran ^[57]. The co-fermented pumpkin contained 1.47% GABA. Bacillus subtilis HA was also used in a two step-fermentation with L. plantarum K154, obtaining a high level of GABA production (about 4800 µg/mL) in a defined medium fortified with glutamate and skim milk ^[58]. Instead, Yang et al. proposed a two-step method to produce GABA from cassava powder using C. glutamicum G01 and L. plantarum GB01-21 ^[27].

In another study, two self-cloned L. plantarum Taj-Apis362 strains possessing high intracellular GAD activity (UPMC90) and high extracellular GAD activity (UPMC91) and a wild-type L. plantarum Taj-Apis362 (UPMC1065) were co-cultured with a starter culture (a mixture of Streptococcus thermophilus and Lactobacillus delbrueckii ssp. bulgaricus) to produce GABA-rich yogurt ^[22].

The wild-type L. plantarum Taj-Apis362 (UPMC1065) was previously isolated from the stomach of a honeybee Apis dorsata ^[51] and used as a host for GAD gene overexpression to produce UPMC90 and UPMC91 strains. After 7 h of fermentation at 39.0 °C, the starter co-culture in skim milk with 2% glucose and 11.5 mM glutamate produces 59.00 mg/100 g of GABA.

Water dropwort (Oenanthe javanica DC), a common aquatic perennial plant widely cultivated in most Southeast Asian countries, was co-fermented with Leuconostoc mesenteroides SM and L. plantarum K154 to produce a novel functional food ingredient enriched with GABA (100 mM) ^[59]. The acidity of the fermented broth, the low concentration of sugar remaining for the second fermentation and the presence of nitrogen sources, stimulated L. plantarum K154 to produce GABA. These data seem to confirm that the production of GABA by bacteria is a bacterial mechanism of response towards acid stress ^[17].

Woraratphoka et al. used a co-culture of L. plantarum L10-11, Lactococcus lactis spp. lactis and L. lactis spp. cremonis in fresh cheese production ^[60]. L. plantarum L10-11 which was isolated from Thai fermented fish (Plaa-som) while Lactococcus lactis spp. lactis and L. lactis spp. cremonis they were commercial strains (Lyofast MWO030, SACCO, Italy). After 18 h the fermented milk by single-L10-11 and co-L10-11 contained 1.21 and 11.30 mg/100 mL of GABA, respectively. Thus, this suggested that in the co-culture test, by transforming lactose into lactic acid, the commercial strains decreased the pH value, creating a favorable condition for the enzymatic activity (GAD) of L. plantarum L10-11 that catalyzes the conversion of glutamate to GABA. Therefore, co-fermentation by L. plantarum L10-11 with other LAB strains could possibly increase the rate of GABA production ^[60].

In a previous study, it was reported that L. plantarum L10-11 was clearly involved in the conversion of MSG to GABA and the highest GABA production was obtained when the initial pH of MRS was in the range of 5.0–6.0 ^[23].

The data emerging from the above studies confirm that the optimal pH for GABA production by L. plantarum is placed in an acidic pH range of 4–6 ^[1].

Zhang et al. evaluated the effects on GABA production by co-culture of Levilactobacillus brevis YSJ3 and L. plantarum JLSC2-6. The results indicate that co-culturing these two strains can improve GABA yield (35.00 ± 1.15 mg/L) in fermented cauliflower stems (Brassica oleracea L. var. botrytis) ^[61].

Functional milk-based beverages enriched with 100 mg/L and 200 mg/L of olive vegetation water phenolic extract (OVWPE) were obtained via fermentation at 40 °C using L. plantarum C48, L. paracasei 15N, S. thermophilus DPPMAST1 and L. delbruecki subsp. bulgarigus DPPMALDb5. The highest amount of GABA (67 mg/L) was detected after 30 days at 4 °C ^[62].

The results obtained from the above studies have shown that co-culture fermentation using L. plantarum with other bacterial species is a novel technology to improve fermentation quality and promote GABA synthesis. The increase in GABA production by L. plantarum in co-culture with other bacteria may be related to the greater availability of nutrients released by the metabolism of the bacterium used in co-cultures ^[27]^[59] which also generates acidic end products of fermentation, which accumulate in the extracellular environment, increasing its acidity and thus promoting GABA synthesis ^[59]^[60]^[61]^[63].

Other studies, cited below, have shown that some L. plantarum strains improve GABA production even when used in co-culture with fungi.

Co-fermentation of L. plantarum K154 and fungus Ceriporia lacerate efficiently produced GABA (15.53 mg/mL) in a defined medium containing 3% glucose, 3% soybean flour, 0.15% MgSO₄, and 5% rice bran for 7 days at 25 °C ^[64].

The increase in GABA production in co-culture could be related to the fact that C. lacerate, thanks to its enzymatic activities (protease, α-amylase, cellulase, β-1,3-glucanase and phosphatase) ^[65], increased the availability of nutrients useful for the growth and survival of L. plantarum.

In a study conducted by Zhang et al., S. cerevisiae SC125 and L. plantarum BC114 were used in co-culture to ferment mulberry (Morus alba L.) and produce a functional beverage enriched with GABA ^[66]. L. plantarum BC114 and S. cerevisiae SC125 were inoculated in pasteurized mulberry substrate with 5 g/L L-glutamate and incubated at 30 °C for 72 h.

Compared to single fermentations with L. plantarum BC114 and S. cerevisiae SC125, which resulted in low GABA production (1.45 g/L and 1.03 g/L, respectively), co-culture produced a higher amount of GABA (2.42 g/L) ^[66].

Therefore, co-cultures of selected fungi with GABA-producing strains belonging to L. plantarum species may be a promising approach for the production of GABA-enriched foods, and therefore, this biotechnological application would also merit further scientific investigation.

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Massimo Iorizzo

Gianluca Paventi

Catello Di Martino

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1. Introduction

2. GABA Production by L. plantarum in Fermented Foods

References