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Review

The Role and Significance of Bacillus and Lactobacillus Species in Thai Fermented Foods

by
Bhagavathi Sundaram Sivamaruthi
1,2,
Karthikeyan Alagarsamy
3,
Natarajan Suganthy
4,
Subramanian Thangaleela
2,
Periyanaina Kesika
1,* and
Chaiyavat Chaiyasut
2,*
1
Office of Research Administration, Chiang Mai University, Chiang Mai 50200, Thailand
2
Innovation Center for Holistic Health, Nutraceuticals, and Cosmeceuticals, Faculty of Pharmacy, Chiang Mai University, Chiang Mai 50200, Thailand
3
Department of Microbiology (Aided), PSG College of Arts & Science, Avinashi Road, Civil Aerodrome Post, Coimbatore 641014, India
4
Bionanomaterials Research Lab, Department of Nanoscience and Technology, Alagappa University, Karaikudi 630003, India
*
Authors to whom correspondence should be addressed.
Fermentation 2022, 8(11), 635; https://doi.org/10.3390/fermentation8110635
Submission received: 16 October 2022 / Revised: 9 November 2022 / Accepted: 9 November 2022 / Published: 12 November 2022
(This article belongs to the Special Issue Bacillus Species and Enzymes)
Browse Figures
Versions Notes

Abstract

:
Fermented foods (FFs) are prepared through controlled or spontaneous microbial growth, promoting the conversion of complex food components by microbial enzymatic action. FFs are common in the cuisine of Southeast Asian countries. Furthermore, FFs have recently become popular worldwide, due to their proposed and proven beneficial health effects. The microbes present in FFs affect the quality, taste, and flavor of the food. Thailand is famous for its versatile range of foods, especially FFs. Fermented beans, fish, meat, sausages, vegetables, and fruits are commonly consumed in Thailand. Thai fermented foods (TFFs) are a key source of bioactive micro-organisms and molecules, and several studies have detailed the isolation, identification, and characterization of potent microbial strains from TFFs; however, a detailed literature review of Bacillus and Lactobacillus species in TFFs is not available. Therefore, in this review, we summarize the available information on representative TFFs, as well as Bacillus and Lactobacillus species in TFFs and their bioactive properties.

1. Introduction

Food and beverages prepared through the growth and metabolic activity of microbes are known as fermented foods (FFs). The fermentation of vegetables, meats, sea and freshwater organisms, dairy, beans, cereals, legumes, and fruits has been documented. The FFs vary in their preparation, as well as their microbial and nutritional composition [1,2]. Fermentation is one of the preferred methods for food preservation (e.g., wine), as the microbes present in the raw materials or developed during fermentation can reduce the threat of pathogenic contamination. The fermentation process also improves the organoleptic properties of some foods [1,3]. FF preparation methods can be divided into two broad categories: natural/spontaneous FFs and culture-dependent FFs. In spontaneous FFs preparation, the microbes present in the raw materials are involved in the fermentation process (e.g., kimchi); meanwhile, in culture-dependent fermentation, a specific starter culture is used to produce FF (e.g., natto, kefir, and so on) [1,4]. Culture-dependent fermentation methods is also practiced by “backslopping,” a method where previous FF is used as a seed for the next production batch [5]. Commercial starter cultures are used to produce FFs with specific organoleptic characteristics (e.g., aroma and taste) [6,7]. However, some traditional FFs (Ka-pi, fish sauce) are still prepared by conventional methods, in order to preserve their quality.
FFs are common in the cuisine and diet of Southeast Asians. The consumption of FFs has been increasing worldwide, due to the scientific proof and awareness that the consumption of FFs can improve the health of consumers [8,9,10,11]. There are several possible mechanisms by which FFs provide beneficial effects to consumers.
The microbial composition of an FF varies, based on the production process, age, packaging and storage, and shelf life [3,7]. The secondary metabolites formed during fermentation may deliver health benefits (e.g., γ-aminobutyric acid, GABA; short-chain fatty acids). The fermentation process aids in converting phenolic compounds into easily available metabolites, reduces toxic compounds and allergens, and enriches the beneficial nutrients (e.g., vitamins) in FFs [1,12].
Fermented soybean (Thua-nao), fermented shrimp paste (Ka-pi), fermented freshwater fish (Pla-ra), milk kefir, fermented pork sausage (Nham), traditional fermented fish products (Plaa-som), fermented sausage (Sai-krog-prieo), fermented beef (Mam), fermented fish with rice (Som-fak), fermented crab (Phu-dong), fermented fish intestine (Sai-pra-mun, Tai-pra), fermented shellfish (Hoi-dong), fermented soybean (Toa-hu-yee, Toa jeaw), pickled green mustard (Phakgard-dong), fermented tea leaves (Bai-maeng), fermented mango (Mamuang-dong), fermented vegetables (Gundruk, Soidon, Suan-tsai, Sayur asin, Paocai), fermented bamboo shoots, sausages, pickled fish, and minced pork are commonly consumed in Thailand [13,14,15,16,17,18,19,20,21,22]. Thai FFs (TFFs) are rich sources of bioactive microbes, such as probiotics [3]. The strains isolated from TFFs have been reported, in terms of their antimicrobial activity, lytic activity, probiotic properties, enzyme, and exopolysaccharide production [3].
The current review provides a brief review of TFFs, with a focus on the role and significance of Bacillus and Lactobacillus species in TFFs.

2. Thai Fermented Foods (TFFs)

Many varieties of traditional fermented beverages and foods are consumed in Thailand. The most common FFs, including soy sauce and Nampla, are consumed in all regions of Thailand; while Thua nao, fermented cooked soybeans, is widely consumed in the northern part of Thailand [23], and Sato, a rice wine made from glutinous rice, is widely consumed in the northeastern region of Thailand [24].
FFs can be generally classified into lactic acid-, fungal-, and alkaline-fermented foods [4]. Generally, the TFFs are classified based on the fermentation type, the raw materials used, the microbes involved, the production technology, and the product usage [25].
Small-scale and cottage levels of traditional TFFs are produced using traditional methods and processes [26]. Raw materials, such as soybean, fish, meat, shrimp, vegetables, rice, and local agricultural products are typically used to prepare FFs. In addition, the unique quality and characteristics of the final product are improved by adding other ingredients. The use of relevant micro-organisms or a starter culture plays an active role in the fermentation process, changing the nutritional, physical, and organoleptic properties of starting materials to enhance the quality, nutritional value, taste, and so on [27]. Some representative TFFs are detailed below, and pictures of the final products are shown in Figure 1.

2.1. Sweet Alcoholic Rice Snack (Khao-mak)

Khao-mak is a low-alcohol sweetened fermented rice, which is a traditional FF made from glutinous rice using a starter called “loog-pang/look-pang Khao-mak”. This traditional fermentation starter is a semi-circular starch ball, made of rice flour containing yeasts and mold inoculum, mixed with herbs such as galangal, garlic, and pepper. To produce this sweet alcoholic rice snack, the rice is soaked and steamed until it is evenly cooked, following which the cooked rice is cooled to room temperature and washed with clean water until the water runs clear. Then, the cooked rice is strained and mixed with powdered loog-pang Khao-mak starter and sugar, and left to ferment at ambient temperatures for 1–3 days. The micro-organisms mainly involved in the fermentation of Khao-mak are yeasts and molds such as Aspergillus spp., Rhizopus spp., Mucor spp., Sa. cerevisiae, and Candida spp. This sweetened fermented rice is consumed without cooking after fermentation [28,29].

2.2. Traditional Sato

Sato is a traditional Thai alcoholic beverage produced by households, especially in rural areas. The preparation of Sato is quite simple, involving rice polishing, steeping, steaming, mixing of the starter culture, fermentation, and separation of high-quality wine from lees. Unlike typical wine fermentation, where natural yeast is found on the fruits, brewing rice wine requires a starter culture (loog pang), in the form of a small ball containing yeast, mold, rice starch, and indigenous spices and herbs, enhancing the unique aroma of Sato [30]. In fact, glutinous rice is soaked in water for 6 to 12 h. Then, the water is drained and the rice is steamed for 30–60 min. The steamed rice is then washed with water and mixed with 0.1–0.2% of powdered starter culture. Next, the mixture is stored in a jar (an earthen jar or a bucket) for 24 to 48 h. After this, water is poured into the rice mixture, which is further fermented for up to two weeks. After fermentation, the content is filtered and is ready for consumption.

2.3. Fermented Fish Product (Pla-ra)

Pla-ra is a famous traditional FF, which is commonly consumed in all parts of Thailand, especially in the North and Northeast. In general, pla-ra is prepared using freshwater fish, such as pearl gourami (Trichogaster leeri), three-spot gourami (Trichogaster trichopterus), java barb (Puntius gonionotus), striped snakehead fish (Channa striata), and so on, or marine fish, such as croaker (Johnius argentatus), cobia (Rachycentron canadum), slender trevally (Caranx leptolepis), and/or short-bodied mackerel (Rastrelliger neglectus). Pla-ra is prepared through the addition of 25–30% salt to the scaled and gutted fish, which is kept for a period of time for natural fermentation, followed by the addition of rice bran, roasted rice, and/or roasted rice bran, then left to further ferment for a period of time. Alternatively, the ingredients are all mixed together at the same time and allowed to naturally ferment for 12–18 months, depending on the desirable organoleptic property, at room temperature (28–30 °C). The fermentation of these raw materials is carried out in a closed-lid container (e.g., an earthen jar or a bucket). Lactic acid bacteria (LAB) are mostly involved in pla-ra fermentation [31]. Rodpai et al. [32] have investigated the microbial diversity of fermented freshwater fish products in pla-ra from three provinces (Khon Kaen, Kalasin, and Roi Et) of northeastern Thailand, and found that Halanaerobium fermentans and/or Tetragenococcus muriaticus (pla-ra samples from Khon Kaen Province), Lactobacillus rennini (pla-ra from Roi Et Province), and T. muriaticus (pla-ra from Kalasin Province) were the dominant bacterial species. The microbial diversity between these samples may be due to the use of different raw materials, salt concentrations, processes, and fermentation durations.

2.4. Fermented Pork Sausage (Nham)

Nham is one of the widely consumed LAB-fermented pork products in Thailand. Thai-style fermented Nham mainly relies on raw material-based adventitious micro-organisms. LAB strains (Lactobacillus plantarum and Pediococcus cerevisiae) and Micrococcus varians are involved in the fermentation of Nham. It is made from ground pork mixed with salt, garlic, ground black pepper, steamed rice, pork rind, and potassium or sodium nitrite. Furthermore, the mixture is packed in banana leaf pockets or cylindrical plastic bags and allowed to ferment at ambient temperatures for 3–5 days, depending on the season. The final pH of the product is around 4.3. The lactic acid produced by LAB ensures the safety of the Nham, as well as intrinsic qualities, including its unique aroma and sour taste [33].

2.5. Fermented Soybean (Thua-nao or Thai Natto)

Thua-nao is a natto-like fermented soybean produced and commonly used in the northern part of Thailand. It is produced by the rural people using a traditional method. In brief, the soybeans are washed, soaked in water overnight, and steamed for 3–4 h. The cooked soybeans are allowed to undergo spontaneous fermentation at ambient temperature for 2–3 days after being placed in bamboo baskets lined and covered with banana leaves [30]. The fermentation of Thua-nao has been attributed to Bacillus spp., where B. subtilis predominates throughout the fermentation process [34,35,36,37].

2.6. Traditional Fermented Tea (Miang)

Miang is a unique type of tea produced in northern Thailand; unlike other types, it is known as an eating or chewing tea. It is a culturally fermented tea leaf with religious significance among northern Thai people. The fermentation process and methods vary considerably among regions. In general, leaves of Camellia sinensis var. assamica are collected and formed into small bundles with bamboo strips for the initial steaming process (1–2 h). After cooling, the individual bundles are tightly pressed and weighted down to ferment naturally in a vinyl bag or banana leaf-lined bamboo basket for 3–4 days to up to a year, depending on the organoleptic evaluation by the producer [38]. Lactobacillus plantarum [39], Enterococcus camelliae [40], Lactobacillus camelliae, Lactobacillus fermentum, Lactobacillus pantheris, Lactobacillus pentosus, Lactobacillus suebicus, Lactobacillus thailandensis, and Pediococcus siamensis have been identified as present in miang samples [41].

2.7. Fermented Minced Fish Cake (Som-fug)

Som-fug, also known as Nham-pla, consists of steamed rice (2–12%), minced garlic (4%), minced fish flesh (78–80%), and salt (2–5%) [42]. The mixture forms a sticky paste and becomes gel-like in appearance when the paste is kneaded. The smaller portions of paste are tightly packed and wrapped in either plastic bags or banana leaves, then left for 3–5 days to ferment at ambient (28–30 °C) or low (4–8 °C) temperature for 5–12 days. L. plantarum, L. brevis, L. fermentum, and P. pentosaceus have been shown to be involved in the fermentation of Som-fug [43,44].

2.8. Fermented Rice Noodles (Khanom-jeen)

Khanom-jeen is one of the most popular traditional fermented foods in Thailand. Thai people widely consume it due to its unique quality and characteristics, such as tenderized texture, sour taste, and flavor. It can be served with various curries, such as green curry with chicken and red curry with fish [45]. The LABs include Lactobacillus spp., Pediococcus spp., and Leuconostoc spp., which are used in the fermentation of Khanom-jeen. It is produced from broken rice by natural fermentation. The rice grains are soaked in water for 1 h and allowed to ferment at ambient temperatures for 2–5 days. The fermented rice is wet-milled and left to precipitate in the tank for 24 h to form a slurry. The resultant flour (slurry) is transferred into a cotton bag overnight, in order to remove excess water. To make noodles, the rice flour is pre-cooked, kneaded, and extruded with an appropriate volume of hot water. Finally, the shaped rice noodles are lined onto either a bamboo basket covered with banana leaves or a plastic sheet.

2.9. Fermented Shrimp Paste (Ka-pi)

Ka-pi is widely consumed as a traditional fermented condiment and seasoning ingredient in Thailand [46]. The shrimp paste (or sauce) is made from small crushed or ground shrimp or krill (Mesopodopsis orientalis), which are mixed with salt in a ratio of 5:1 w/w [47]. The mixture is stored in jars and sun-dried for months at ambient temperatures, until the development of a unique aroma. Furthermore, ka-pi fermentation greatly depends upon the natural microbiota, raw materials, production method, and production environment, without the use of a starter culture [48]. Strains of Aerococcaceae, Bacillaceae, Enterococcaceae, and Staphylococcaceae are largely involved in the production of ka-pi. Ka-pi has been reported to include osmotic stress-tolerant gram-positive bacteria, which can tolerate a high salinity of 13.6–39.0% [49].

2.10. Fermented Fish Paste (Ka-pi-plaa)

Ka-pi-plaa is a popular traditional fermented fish paste in Northeastern and Southern Thailand. It is typically added as a condiment in various dishes, in order to enhance the palatability of foods [50]. Generally, to prepare Ka-pi-plaa, whole or eviscerated fish are mixed with 15–25% salt and compacted, then naturally fermented for 10 days at ambient temperatures (28–30 °C) under anaerobic conditions [51]. Depending on the autolytic and enzymatic actions during fermentation, the consistency of the fish paste may vary from hard, soft, and pasty to dry, being dark grayish brown to gray in color [52,53]. Halophilic bacteria are mainly involved in the fermentation of ka-pi-plaa.

2.11. Thai Pickled Vegetables (Phak-dong)

Phak-dong is a pickled vegetable consumed in Thailand [54]. In brief, sliced vegetables are covered with hot pickling brine (about 8–22% salt) in a jar and brought to a boil over medium to high heat. Then, the water is drained off, and a 3% sugar solution is added. The mixture is then fermented at room temperature for three to five days. The fermentation is produced by naturally occurring LAB, including L. fermentum, L. casei, L. paracasei, L. brevis, L. plantarum, W. koreenis, W. cibaria, and W. confuse [3]. The sensory characteristics of phak-dong and the dietary benefits can be preserved by following the standard method of lactic acid-mediated fermentation [55].

3. Prevalence of Bacillus and Lactobacillus Species in Thai Fermented Foods

3.1. Bacillus Strains in Thai Fermented Foods

A Bacillus strain has been isolated from Thai fermented soybeans (Thua-nao), which was identified as B. licheniformis. This strain possesses mycotoxin-degrading properties [13], and approximately 74% and 92.5% decreases in aflatoxin B1 and ochratoxin A were observed, respectively. As such, this study claimed that B. licheniformis could reduce the mycotoxin levels in fermented soybean products [13].
A novel Bacillus strain (SKP7-4T) has been reported to be isolated from Thai shrimp paste (Ka-pi). In detail, the genome of the SKP7-4T strain was 4.68 Mb in size with 5208 coding sequences. The strain is closely related to B. vietnamensis JCM 11124T, B. marisflavi JCM 11544T, B. aquimaris JCM 11545T, and B. oryzaecorticis JCM 19602T, with more than 97% similarity. Based on the analysis, the study claimed that SKP7-4T belongs to the Bacillus genus, with the proposed name of B. salacetis sp. nov. [14]. The microbiological screening of Ka-pi samples available in a wet market and supermarkets in Thailand showed that wet market samples were richer in Bacillus strains [56].
Through next-generation sequencing, samples of Thai fermented freshwater fish (Pla-ra) have been screened for microbial load. Bacillus species were detected in the samples, and about 600 genomes were detected with protease and aminopeptidase coding genes. Among the screened samples, the highest number of aminopeptidase and protease genes were detected in Bacillus spp. Along with Bacillus spp., several other microbes were detected in Pla-ra [57].
Bacterial composition analysis of Northern TFFs has shown that Thua-nao is rich in Bacillus spp. [57] Similarly, Thua-nao samples collected from Lao PDR and Thailand have been screened for microbiological quality, and B. cereus strains were detected in 27 samples. The emetic toxin-coding gene was detected in some of the strains. The study results indicated that naturally fermented Thua-nao requires hygienic procedures to maintain food safety [58].
The prevalence of pathogens on pla-ra production containers (clay and polyethylene) was studied. Among 110 samples from 25 pla-ra containers, 20–30% of samples were reported to host B. cereus strains. They also reported the presence of Klebsiella aerogenes (K. aerogenes), Cl. perfringens, E. coli, Listeria innocua (Li. innocua), and Staphylococcus aureus [59].
Bacterial isolates have been isolated from TFFs milk kefir. Of about 85 isolates, 25 isolates belonged to Bacillus sp. A 16S rRNA-based analysis suggested that five isolates had 100% similarity to B. amyloliquefaciens SD-32, Bacillus sp. LB15, Bacillus sp. L_D12_A_P, Bacillus sp. C87, and B. methylotrophicus 3B_1.1. All isolates (Bacillus spp.) were also reported to produce exopolysaccharides [16].
Bacillus strains isolated from Salt-fermented fish (Pla-ra) have been characterized. These isolates were identified as B. velezensis (6-2), B. amyloliquefaciens (78-1), and B. infantis (63-11). B. velezensis has stress-resistant and acid-tolerant proteins. B. amyloliquefaciens possesses epithelial layer adhesion proteins. B. infantis presented antimicrobial activity. Hemolysin-coding genes were also found in the isolates [60].

3.2. Lactobacillus Strains in Thai Fermented Foods

A Lactobacillus strain has been isolated from Thai fermented fruits and vegetables. Biochemical and 16S rRNA gene sequencing profile analyses allowed for the identification of the strain (L. plantarum) [17].
L. plantarum BCC 9546 isolates have been isolated from Nham, a Thai fermented pork sausage, where the acid production and H+-ATPase activity were lower than in the wild-type. The isolates were acid-sensitive, and the strain could reduce post-acidification severity at room temperature [16,18]. Similarly, Ratanaburee et al. [61] have reported a GABA-producing L. namurensis strain isolated from Nham.
Lactic acid bacteria (LAB) strains have been isolated from a traditional fermented fish product (Plaa-som). L. plantarum, L. fermentum, and other strains were found to be predominant in Plaa-som. The study claimed that these strains could be used as a starter culture to produce Plaa-som [19]. Lactobacillus species have been isolated from Thai fermented freshwater fish (Pla-ra). The microbial content of pla-ra influences the associated glutamyl peptide generation. Along with Tetragenococcus and Lentibacillus species, Lactobacillus species were also found in pla-ra [62].
Several Thai fermented products (91 samples) and kefir (2 samples) have been screened for potent LABs. The isolates were studied according to their probiotic properties, and the isolates were found to be L. plantarum, L. pentosus, and L. brevis. This study claimed that these strains could be used alternatives to both antibiotics and chemical preservatives [20].
L. plantarum L10-11 has been isolated from Thai fermented fish (Plaa-som), which was found to be a γ-aminobutyric acid (GABA) producer. This strain was used to produce Thai fermented vegetables (Som-pak), and it was shown that the production of Som-pak using L10-11 led to a high acceptability rate [63].
LAB strains have been isolated from the Thai fermented product Pak-sian, which were later identified as P. pentosaceus, Lactiplantibacillus plantarum, Levilactobacillus brevis, and L. fermentum. They were able to survive in acidic conditions and exhibited antibacterial activity. The Lactobacillus strains were susceptible to antibiotics (chloramphenicol, rifampicin, and ampicillin). The LABs were non-hemolytic and non-biogenic amine producers. Based on the adhesion capacity, L. fermentum SK324, and Levi. brevis SK335 were found to be the better probiotic strains among the LAB isolates [64].
LAB strains have been isolated from several TFFs. LABs isolated from bamboo shoot pickles and pla-ra exhibited high tolerance to gastric conditions. L. fermentum K4 is one of these isolates, which showed high antimicrobial activity, surface hydrophobicity, and resistance to nalidixic acid and clindamycin. The study concluded that L. fermentum K4 could be a potent probiotic candidate [21]. Similarly, L. plantarum P10 has been isolated from TFFs, and it was claimed that the strain could be an effective probiotic candidate [22].

4. Enzymes and Bioactive Peptides of Bacillus and Lactobacillus Species in Thai Fermented Foods

4.1. Bioactive Peptides (Bacteriocin-like Substances)

B. siamensis B44v, isolated from Thai pickled vegetables, has exhibited bacteriocin-like activity against Aeromonas hydrophila (A. hydrophila) and Streptococcus agalactiae. Proteinase K treatment completely nullified the antagonistic action of the supernatant of B44v, but not lipase, glucoamylase, and α-amylase treatments, which indicated that a proteinaceous substance was responsible for the inhibitory property of B44v [54].
The bacteriocin KTH0-1S is heat stable, with a molecular mass of 3.346 kDa. Molecular sequencing and PCR studies have shown that the bacteriocin KTH0-1S is nisin Z [65].
The bacteriocin produced by L. plantarum PMU33 is heat stable and active in a broad pH range (2–10); furthermore, mass spectrometry analysis revealed that the molecular masses of the two peptides comprising the bacteriocin are 3222 and 3099 Da. The bacteriocin was similar to the two-peptide plantaricin W, as confirmed by a PCR-based study [66].
The bacteriocin produced by L. plantarum subsp. plantarum SKI19 inhibited closely related species and Listeria monocytogenes DMST 17303 [67]. Similarly, L. fermentum P43-01 presented antibacterial activity against Helicobacter pylori (He. pylori), where the inhibitory activity was associated with bacteriocin-like compounds which are sensitive to α-chymotrypsin and pepsin [68].
The antimicrobial substances produced by L. fermentum RB01-SO have been shown to be sensitive to proteolytic enzymes. The production of those compounds was higher when RB01-SO was cultured in MRS broth with 1% NaCl at pH 7 [69].
The reported bacteriocin-like substance-producing strains showed antimicrobial activities against several severe foodborne pathogens.

4.2. Enzymes

The crude enzymes of B. subtilis DB, isolated from Thua Nao, were capable of hydrolyzing β-lactoglobulin (a known allergen present in milk) at the Gln35-Ser36 position, while B. subtilis DB and SR strains could hydrolyze gliadin (an allergen present in wheat). The enzymes could be used to prepare hypoallergic wheat or dairy products [70]. Lipase-producing Bacillus strains have been reported. The lipase production was observed in broth in the presence of Tween under the following optimal conditions: Temperature, 40 °C; pH, 7.5; and 30 h of incubation. The potent lipase-producing strain was found to be B. subtilis SS48-5 [71].
LAB strains isolated from TFFs have been shown to produce L-glutaminase and glutamic acid decarboxylase (GAD) enzymes. A total of 22 LAB strains were glutaminase producers, with three strains producing extracellular enzymes, twelve strains producing intracellular, and seven strains producing cell wall-associated enzymes. Seventeen LABs were found to be likely GAD producers. Potent L-glutaminase and GAD producers were identified as L. brevis and L. fermentum, respectively [72]. Further, the production of L-glutamic acid (GA) and GABA-rich fermented food using L. brevis and L. fermentum strains has been reported. The co-factor K2HPO4 influences GA production, while pH and temperature affect GABA production during Hericium erinaceus fermentation [73]. The LAB strains with likely glutamate decarboxylase genes, which can produce GAD enzymes, were isolated and identified as L. plantarum [74] and L. brevis GPB7-4 [75].
L. futsaii CS3, isolated from Thai fermented shrimp products (Kung-Som), produces high GABA in the medium and during the fermentation process of Kung-Som in the presence of monosodium glutamate (MSG). However, the enzyme profile was not reported [76,77]. Similarly, L. namurensis NH2 [78], L. plantarum L10-11 [64], Levi. brevis F064A [79], and L. plantarum DW12 [80] produce GABA during the fermentation process; however, knowledge of the enzymes involved in the process is lacking.
Toyokawa et al. [81] have reported the proteolytic enzyme-producing B. licheniformis RKK-04, which was isolated from Thai fermented fish sauce. The molecular mass of the enzyme was 31 kDa with an isoelectric point of >9.3. The optimum condition for the enzyme was pH 10 and 50 °C, and phenylmethanesulfonyl fluoride and di-isopropyl fluorophosphate inhibited the enzyme activity, suggesting that the enzyme belongs to subtilisin-like alkaline serine proteinase family, with unique cleavage sites in the oxidized insulin B-chain. The halotolerant proteinase (which remained active at 30% NaCl) can break down fish proteins; thus, this enzyme may be an active player in fish sauce production.

5. Bioactivities of Bacillus and Lactobacillus Strains Isolated from Thai Fermented Foods

5.1. Bioactivities of Bacillus Strains

B. siamensis B44v, isolated from Thai pickled vegetables (Phak-dong), has presented antibacterial activities, especially against fish pathogens (A. hydrophila and Streptococcus agalactiae). B44v showed susceptibility to commonly used antibiotics, indicating that this strain is not an antibiotic-resistant bacterium. B44v exhibited probiotic properties, such as the ability to survive in gastric juice, hydrophobicity, auto-agglutination, co-aggregation, and mucin binding. Furthermore, B. siamensis B44v produced protease and cellulase enzymes. B44v showed probiotic-like activities in catfish culture, improving survivability and growth. Additionally, B44v showed protection against A. hydrophila infection in catfish. The study suggested that B. siamensis B44v could act as a probiotic in aquaculture settings [54]. Likely, B. subtilis var. Thua-nao-mediated fermented soybeans (Thua-nao) were rich in flavonoid and phenolic contents, and presented good antioxidant activities. The thua-nao extract presented high genistein and daidzein contents. The isoflavone from Thua-nao showed cancer cell (MCF-7 and HEK293) inhibition ability. This study suggested that the antioxidant-rich Thua-nao could be considered as a therapeutic food supplement [82].
Thua-nao (fermented soybean) has been fermented with B. subtilis TN51, where B. subtilis TN51-mediated fermentation improved the flavonoid and phenolic contents, as well as free-radical scavenging activity. These results suggested that TN51-mediated fermented Thua-nao could serve as a functional food with improved antioxidant activity [83].
γ-Glutamyl hydrolase (28 kDa) has been purified from a culture broth of Bacillus sp. isolated from Thai Thua-nao, a natto-like fermented soybean food [84]. B. licheniformis RKK-04 has been isolated from fermented fish sauce broth, which produces high proteolytic and halotolerant serine proteinase [81].
Phromraksa et al. [70] have isolated B. subtilis and B. licheniformis strains from Thua-nao, and showed that they could reduce the allergenicity of gliadin and β-lactoglobulin through hydrolysis. The results indicated that B. subtilis could be used to produce hypoallergenic food products.

5.2. Bioactivities of Lactobacillus Strains

5.2.1. Antimicrobial Activity

About 12,520 LB strains have been isolated from Thai fermented fish products (Som-fak) and screened for bacteriocin production. A broad-spectrum antimicrobial agent, heat-stable bacteriocin-like substance (active against food-borne pathogens)-producing strain was selected, which was found to be L. plantarum PMU33 [66]. The molecular mass of the bacteriocin was similar to that of two-peptide plantaricin W (Plow). PCR analysis confirmed that PMU33 possesses plwα and plwβ genes. The results of the study suggested that the bacteriocin-producing L. plantarum PMU33 could be used as a bio-preservative agent [66]. Likewise, the heat-stable bacteriocin-producing La. lactis KTH0-1S has been isolated from Thai traditional fermented shrimp (Kung-som). The associated bacteriocin could inhibit food-spoiling microbes; especially inhibiting the growth of Staphylococcus aureus. The bacteriocin was stable at different pH levels and high temperatures while being sensitive to proteolytic enzymes. KTH0-1S is a safe and bacteriocinogenic strain, which may be used as an antimicrobial agent in producing fermented seafood products [65].
LAB strains isolated from Thai fermented pork sausage have been screened for antimicrobial activity against L. sakei subsp. sakei JCM 1157. A potent strain was identified as L. plantarum subsp. plantarum SKI19, which produces bacteriocin-like substances that inhibit closely related species as well as Li. monocytogenes DMST 17303, E. coli DMST 4212, and Staphylococcus aureus DMST 8840). SKI19 can survive under gastric conditions and adhere to cell surfaces. The strain SKI19 is a non-hemolytic, non-biogenic amine producer which is susceptible to antibiotics, suggesting that SKI19 could be a probiotic strain used in fermented food production [67].
LAB strains have been isolated from traditional Thai fermented rice noodles (Khanom-jeen). Some of the strains were identified as L. paracasei subsp. tolerans, L. fermentum, L. plantarum subsp. plantarum, and L. pentosus. L. fermentum P43-01 exhibited antimicrobial activity against Helicobacter pylori (He. pylori) strains MS83 and BK364, due to the production of bacteriocin-like proteinaceous compounds, which were sensitive to pepsin and α-chymotrypsin. This study showed that P43-01 may be used as a probiotic to improve the health span of He. pylori-infected patients [68].
The strain RB01-SO, isolated from Thai fermented vegetables, has presented antimicrobial activity against Streptococcus suis, E. coli, B. subtilis, Staphylococcus aureus, Streptococcus agalactiae, Vibrio harveyi (V. harveyi), La. lactis, En. faecalis, Micrococcus luteus (M. luteus), Li. innocua, Li. monocytogenes, Pseudomonas aeruginosa (Ps. aeruginosa), Salmonella sp., A. veronii, and L. sakei. This study showed that the antagonistic property of RB01-SO was related to the production of stable bacteriocin-like substances. LAB strains with anti-S. suis properties are particularly promising for the production of food or feed [69].

5.2.2. GABA-producing Strains

Woraharn et al. [72] have screened LAB strains isolated from TFFs to find L-glutaminase and GAD-producing strains. These LAB strains were identified as relatives of L. brevis ATCC 14869 and L. fermentum NBRC 3956. Using L. brevis HP2 and L. fermentum HP3 improved the production of fermented H. erinaceus enriched with GA and GABA [85].
L. futsaii CS3 has been isolated from Thai fermented shrimp (Kung-Som) and characterized. This strain could be a potent candidate for producing GABA-rich FFs [76,77]. Later, Kung-Som was prepared with L. futsaii CS3, in order to improve its GABA content. Further fermentation conditional optimization and microbiological evaluation suggested that L. futsaii CS3 could be a compelling starter culture for safe and quick GABA-rich Kung-Som production [86].
Thai fermented pork sausage (Nham) has been prepared using L. namurensis NH2 and P. pentosaceus as starter cultures. The cholesterol (35%) and seven biogenic amine levels were reduced in Nham. The study revealed that the production of Nham using GABA-producers as starters could improve the quality of the product, in terms of biogenic amine and cholesterol contents [87].
GABA-producing LAB strains (P. pentosaceus HN8 and L. namurensis NH2) have been used as starter cultures to produce Nham (Thai fermented pork sausage). The Nham was prepared with 106 CFU/g of HN8 and NH2 strains, as well as 0.5% MSG, and showed high content of GABA. The resulting Nham also exhibited high sensory acceptability [61].
LAB isolates of Thai fermented fish products (Plaa-som) have been screened for GABA production. L10-11 showed high GABA production in de Man, Rogosa, and Sharpe medium with monosodium glutamate (MSG). The addition of NaCl did not inhibit GABA production. L10-11 was identified as L. plantarum L10-11, and the use of L10-11 increased the acceptability of the product. The study showed that L. plantarum L10-11 could improve the quality of the final product [62]. Similarly, Levi. brevis F064A has been isolated from Thai fermented sausages. F064A has been proven as a GABA-producing strain [79]. F064A can tolerate bile acids and acidic pH conditions, indicating its probiotic nature. Mulberry fruit juice (MFJ) was prepared using 5% inoculation of F064A as a starter culture with 2% MSG. After 48 h of fermentation, the MFJ showed high GABA content, increased antioxidant activity, and antagonistic activity against Bacillus, Salmonella, and Shigella species. The prepared MFJ was claimed to be a potent functional food [88].
LAB isolates have been obtained from various Thai fermented products—including pickled Brassica oleracea, Lasia spinosa (L.) Thwaites, Crateva adansonii subsp. trifoliata Roxb., Allium ascalonicum, and fermented pork—and were screened for GABA production. The potent strains were found to be L. plantarum subsp. plantarum, L. argentoratensis, L. pentosus, and L. fermentum. Molecular screening indicated the presence of glutamate decarboxylase genes (gadA) in L. plantarum [74]. Similarly, Pakdeeto et al. [75] have reported GABA-producing LAB strains isolated from Thai fermented bamboo shoots, salted mango, pickled green mustard, and sweetened radish. The strains were closely related to L. brevis, L. plantarum, L. fermentum, and L. pentosus. Molecular screening identified that L. brevis GPB7-4 harbors the gadA and gadB genes.
LAB strains have been screened for GABA production, and the predominant strain was identified as L. plantarum DW12. A functional fermented red seaweed beverage was prepared using DW12, and the conditions required to achieve high GABA content were standardized [80].

5.2.3. Starter Culture to Prepare Fermented Foods

LAB strains—especially Lactobacillus strains isolated from TFFs—have been further used to produce FFs. For example, Nham has been prepared with LAB strains (L. sakei BCC102 and Debaryomyces hansenii BCC 106) previously isolated from Nham. The use of a starter culture significantly reduced the total biogenic amine content in sausages, compared to the control, possibly due to the rapid pH drop during fermentation. The study suggested that using decarboxylase-negative LABs in starter cultures was an important factor to consider during the production of Nham [89]. LAB strains isolated from raw goat’s milk, pla-som (fermented fish), tua-nao (alkaline fermented soybean), pickled garlic and cabbage, Miang (fermented tea leaf product), and kimchi have been screened for probiotic properties. The strains with high bile salt and acid tolerance were further screened for antimicrobial activities against foodborne pathogens. The strains were identified as L. fermentum and L. plantarum. L. plantarum demonstrated high adhesion ability and was non-cytotoxic against Caco-2 cells. Chèvre Cheese produced using L. plantarum exhibited high shelf life and stability [90]. LAB strains isolated from fermented Pak-sian (Thai traditional vegetables) have been screened, some of which were identified as Levilactobacillus brevis and L. fermentum. Lactobacillus strains are susceptible to antibiotics, and are non-biogenic amine producers and non-hemolytic strains. Levi. brevis and L. fermentum exhibited high adhesion properties. The author suggested that these strains could be used as a starter culture to produce functional fermented Pak-Sian [64].
LAB strains (L. plantarum IFRPD P15 and L. reuteri IFRPD P17) isolated from naturally fermented Plaa-som have been further used to produce Plaa-som. IFRPD P15 was a strong acid producer, while IFRPD P17 inhibited the growth of pathogens. The study claimed that using a mixture of LAB strains could produce Plaa-som in a shorter fermentation time [91]. A list of Bacillus and Lactobacillus strains isolated from TFFs is provided in Table 1.

5.2.4. Other Activities

L. brevis TBRC 3003, isolated from naturally fermented Thai pickled vegetable, has been studied for its cytotoxic effects. L. brevis TBRC 3003 exhibited the highest cytotoxicity against HepG2 cells and showed colony inhibition activity against MCF-7 cells. The results indicated that TBRC 3003 could be used to prepare functional foods, which may act against liver and breast cancers [92].
LAB strains isolated from TFFs (water kefir, fermented vegetable products) have been reported to have psychobiotic effects. In fact, multi-strain probiotic supplementation (6 × 109 CFU) improved locomotor function, anxiety, and short-term memory in a rodent model. Probiotic supplementation improved the antioxidant system in rat brains and exhibited neuroprotective effects. The results showed that probiotic supplements could improve behavior [93]. Furthermore, probiotics decrease anxiety and improve neuroplasticity. Psychobiotics-based functional foods may promote improved human behavior [94].
L. paraplantarum L34b-2 isolated from Thai fermented beef improved growth, disease resistance, and immunity in Pangasius bocourti. The L34b-2 strain has the characteristic features of probiotics, including bacteriocin-like activity, tolerance for gastric conditions, adhesion ability, non-hemolytic, and susceptibility to antibiotics. The supplementation of L34b-2 improved the growth rate and weight gain in catfish and increased their immunity against A. hydrophila FW52 [95].
In another study, LAB strains isolated from FFs were screened for their antibacterial activity against fish pathogens (Streptococcus agalactiae, A. caviae, and A. hydrophila). The potent isolate (CR1T5) was found to be L. plantarum, which could tolerate gastric juice, adhere to the mucosal layer, and be non-hemolytic. Tilapia fish (Oreochromis niloticus) supplemented with L. plantarum showed growth improvement with no mortality, and the pathogen-challenged CR1T5-fed fish showed higher survival rates. These results indicate that L. plantarum CR1T5 could be a promising probiotic for aquaculture [96].
LAB strains have been isolated from fermented pork and fermented tea, and were assessed for their probiotic properties. Three LAB isolates from the fermented pork showed high adhesive properties and antimicrobial activity against pathogens. These strains were identified as L. fermentum, and were sensitive to common antibiotics but resistant to vancomycin and ciprofloxacin [97]. The representative bioactivities of Bacillus and Lactobacillus species in TFFs are depicted in Figure 2.

6. Conclusions

Several Thai FFs have not yet been explored, in terms of their chemical and biological compositions. The reproducibility of TFFs, with their unique organoleptic properties, relies on the microbes, raw materials used, and production methods. Still, the traditional production of some TFFs has not yet been reported on scientific platforms.
In this paper, bioactive peptides (bacteriocin-like substances) and enzymes (L-glutaminase, GAD, hydrolase, proteolytic enzyme) produced by Bacillus and Lactobacillus strains in TFFs were detailed. Various studies have discussed the antibacterial, anti-allergic, antioxidant, and cytotoxic activities of Bacillus and Lactobacillus strains. Moreover, these strains have been documented as probiotics, psychobiotics, and neuromodulators; however, the development of subsequent functional foods using bioactive isolates remains limited.
The current literature survey demonstrated that further extensive studies are needed to reveal the bioactivities of under-explored TFFs. The use of natural bioactive microbes in the food industry might facilitate the development of potent functional foods.

Author Contributions

Conceptualization, B.S.S., P.K. and C.C.; methodology, B.S.S. and K.A.; validation, B.S.S., P.K. and C.C.; formal analysis, K.A., N.S., B.S.S. and S.T.; investigation, K.A., P.K. and B.S.S.; resources, C.C.; writing—original draft preparation, B.S.S., K.A., P.K. and C.C.; writing—review and editing, B.S.S., K.A., N.S., P.K. and C.C.; supervision, C.C. and B.S.S.; project administration, C.C.; funding, C.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received funding from Chiang Mai University, Thailand.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We wish to thank Chiang Mai University, Chiang Mai, Thailand. The Chiang Mai University, Chiang Mai, Thailand, partially supported the study. S.T thankfully acknowledges the CMU Post-doctoral fellowship for its support.

Conflicts of Interest

The authors declare no conflict of interest.

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Fermentation 08 00635 g001 550
Figure 1. Representative Thai fermented foods: (a) Khao-mak; (b) Sato; (c) Pla-ra; (d) Nham; (e) Thua-nao or Thai natto; (f) Miang; (g) Som-fug; (h) Khanom-jeen; (i) Ka-pi; (j) Ka-pi-plaa; and (k) Phak-dong. The pictures were captured at the local market of Chiang Mai, Thailand.
Figure 1. Representative Thai fermented foods: (a) Khao-mak; (b) Sato; (c) Pla-ra; (d) Nham; (e) Thua-nao or Thai natto; (f) Miang; (g) Som-fug; (h) Khanom-jeen; (i) Ka-pi; (j) Ka-pi-plaa; and (k) Phak-dong. The pictures were captured at the local market of Chiang Mai, Thailand.
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Fermentation 08 00635 g002 550
Figure 2. Representative bioactive properties of Bacillus and Lactobacillus species found in Thai fermented foods (The figure has been created using BioRender.com; accessed on 14 September 2022).
Figure 2. Representative bioactive properties of Bacillus and Lactobacillus species found in Thai fermented foods (The figure has been created using BioRender.com; accessed on 14 September 2022).
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Table
Table 1. Bacillus and Lactobacillus species isolated from Thai fermented foods.
Table 1. Bacillus and Lactobacillus species isolated from Thai fermented foods.
Fermented foodsIsolatesRemarksRef.
Bacillus species
Thai fermented soybean (Thua-nao)B. licheniformisInhibits Aspergillus strains.
Reduces AFB1 and OTA levels.		[13]
Thai fermented shrimp paste (Ka-pi)B. salacetis sp. nov.Novel isolate from Ka-pi, Gram+, aerobic, slightly halophilic, and
endospore-forming bacterium.		[14]
Thai fermented foods (Milk kefir)B. amyloliquefaciens SD-32, Bacillus sp. LB15, Bacillus sp. L_D12_A_P, Bacillus sp. C87, B. methylotrophicus 3B_1.1, and other 20 Bacillus spp.EPS-producing strains.[16]
Thai fermented shrimp paste (Ka-pi)Bacillus species-[56]
Thai fermented freshwater fish (Pla-ra)Bacillus spp.Low abundance.
Strain with aminopeptidase and
protease genes.		[57]
Thua-naoBacillus spp.Predominantly found in Thua-nao.[58]
Thua-naoB. cereusPathogenic strain.
Toxin-coding gene was detected.		[59]
Pla-ra *B. cereus20–30% of samples contain B. cereus.[60]
Salt-fermented fish (Pla-ra)B. velezensis, B. amyloliquefaciens, and B. infantisStress-resistant and acid-tolerant.
Antimicrobial activity.
Bacteriocin coding gene present.		[61]
Lactobacillus species
Pla-raLactobacillus species-[15]
Fermented fruits and vegetablesL. plantarum-[17]
Thai fermented pork sausage (Nham)L. plantarum BCC 9546Neomycin-resistant mutants.
Acid-sensitive strain.		[18]
Thai traditional fermented fish product (Plaa-som)L. plantarum, and L. fermentum.-[19]
Fermented sausage (Sai-krog-prieo), fermented beef (Mam), Nham, fermented shrimp (Pla-som) and fish with rice (Som-fak), Pla-ra, fermented crab (Phu-dong), fermented fish intestine (Sai-pra-mun; Tai-pra), fermented shellfish (Hoi-dong), fermented soybean (Toa-hu-yee; Toa jeaw), pickled green mustard (Phakgard-dong), fermented tea leaves (Bai-maeng), fermented mango (Mamuang-dong), and KefirL. plantarum, L. pentosus, L. brevisAntimicrobial activity [20]
Pla-ra, Thai fermented pork, Pha-gard-dorng, bamboo shoots and ginger pickles. L. fermentum K4Probiotic strain[21]
Pickled fish, kimchi, crab, minced fish, sausages and Nham.L. plantarum P10Probiotic strain[22]
Thai fermented pork sausage (Nham)L. namurensisGABA producer[61]
Thai fermented fish (Plaa-som)L. plantarum L10-11GABA producer[63]
Thai fermented product (Pak-sian)Lactiplantibacillus plantarum,
L. fermentum SK324.		Probiotic strains[64]
Bacillus: B; Lactobacillus: L; AFB1: Aflatoxin B1; OTA: Ochratoxin A; GABA: Gamma-aminobutyric acid. EPS: Exopolysaccharide. GABA: γ-aminobutyric acid. * Samples collected from the Pla-ra manufacturing containers.
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Sivamaruthi, B.S.; Alagarsamy, K.; Suganthy, N.; Thangaleela, S.; Kesika, P.; Chaiyasut, C. The Role and Significance of Bacillus and Lactobacillus Species in Thai Fermented Foods. Fermentation 2022, 8, 635. https://doi.org/10.3390/fermentation8110635

AMA Style

Sivamaruthi BS, Alagarsamy K, Suganthy N, Thangaleela S, Kesika P, Chaiyasut C. The Role and Significance of Bacillus and Lactobacillus Species in Thai Fermented Foods. Fermentation. 2022; 8(11):635. https://doi.org/10.3390/fermentation8110635

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Sivamaruthi, Bhagavathi Sundaram, Karthikeyan Alagarsamy, Natarajan Suganthy, Subramanian Thangaleela, Periyanaina Kesika, and Chaiyavat Chaiyasut. 2022. "The Role and Significance of Bacillus and Lactobacillus Species in Thai Fermented Foods" Fermentation 8, no. 11: 635. https://doi.org/10.3390/fermentation8110635

APA Style

Sivamaruthi, B. S., Alagarsamy, K., Suganthy, N., Thangaleela, S., Kesika, P., & Chaiyasut, C. (2022). The Role and Significance of Bacillus and Lactobacillus Species in Thai Fermented Foods. Fermentation, 8(11), 635. https://doi.org/10.3390/fermentation8110635

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