Thai Fermented Foods as a Versatile Source of Bioactive Microorganisms—A Comprehensive Review
Abstract
:1. Introduction
2. Bioactive Microbes from Thai Fermented Foods
2.1. Strains with Antimicrobial Properties
2.2. Lytic Activity
2.3. Probiotic Strains
2.4. Enzyme Production
2.5. Gamma-Aminobutyric Acid (GABA) Production
2.6. Exopolysaccharide (EPS) Production
3. Conclusions and Future Prospects
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Tamang, J.P. Himalayan Fermented Foods: Microbiology, Nutrition and Ethnic Values, 1st ed.; CRC Press: New Delhi, India, 2009; pp. 1–216. ISBN 9781420093247. [Google Scholar]
- Yan, P.M.; Xue, W.T.; Tan, S.S.; Zhang, H.; Chang, X.H. Effect of inoculating lactic acid bacteria starter cultures on the nitrite concentration of fermenting Chinese Paocai. Food Control 2008, 19, 50–55. [Google Scholar] [CrossRef]
- Puspito, H.; Fleet, G.H. Microbiology of sayur asin fermentation. Appl. Microbiol. Biotechnol. 1985, 22, 442–445. [Google Scholar] [CrossRef]
- Viander, B.; Maki, M.; Palva, A. Impact of low salt concentration, salt quality on natural large-scale sauerkraut fermentation. Food Microbiol. 2003, 20, 391–395. [Google Scholar] [CrossRef]
- Chen, Y.S.; Yanagida, F.; Hsu, J.S. Isolation and characterization of lactic acid bacteria from suan-tsai (fermented mustard), a traditional fermented food in Taiwan. J. Appl. Microbiol. 2006, 101, 125–130. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.S.; Wu, H.C.; Lo, H.Y.; Lin, W.C.; Hsu, W.H.; Lin, C.W.; Lin, P.Y.; Yanagida, F. Isolation and characterization of lactic acid bacteria from jiang-gua (fermented cucumbers), a traditional fermented food in Taiwan. J. Sci. Food Agric. 2012, 92, 2069–2075. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.S.; Wu, H.C.; Pan, S.F.; Lin, B.; Lin, Y.H.; Tung, W.C.; Li, Y.; Chiang, C.; Yanagida, F. Isolation and characterization of lactic acid bacteria from yan-taozih (pickled peaches) in Taiwan. Ann. Microbiol. 2013, 63, 607–614. [Google Scholar] [CrossRef]
- Chen, Y.S.; Wu, H.C.; Wang, C.M.; Lin, C.C.; Chen, Y.T.; Jhong, Y.J.; Yanagida, F. Isolation and characterization of lactic acid bacteria from pobuzihi (fermented cummingcordia), a traditional fermented food in Taiwan. Folia Microbiol. 2013, 58, 103–109. [Google Scholar] [CrossRef] [PubMed]
- Chang, C.H.; Chen, Y.S.; Yanagida, F. Isolation and characterization of lactic acid bacteria from yan-jiang (fermented ginger), a traditional fermented food in Taiwan. J. Sci. Food Agric. 2011, 91, 1746–1750. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, D.T.; van Hoorde, K.; Cnockaert, M.; de Brandt, E.; Aerts, M.; Binh Thanh, L.; Vandamme, P. A description of the lactic acid bacteria microbiota associated with the production of traditional fermented vegetables in Vietnam. Int. J. Food Microbiol. 2013, 163, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Karovicova, J.; Kohajdova, Z.; Greif, G. The use of PCA, CA, FA for evaluation of vegetable juices processed by lactic acid fermentation. Czech J. Food Sci. 2002, 20, 135–143. [Google Scholar] [CrossRef]
- Tanasupawat, S.; Komagata, K. Lactic acid bacteria in fermented foods in Thailand. World J. Microbiol. Biotechnol. 1995, 11, 253–256. [Google Scholar] [CrossRef] [PubMed]
- Swain, M.R.; Anandharaj, M.; Ray, R.C.; Rani, R.P. Fermented fruits and vegetables of Asia: A potential source of probiotics. Biotechnol. Res. Int. 2014, 2014, 19. [Google Scholar] [CrossRef] [PubMed]
- Demir, N.; Bahceci, K.S.; Acar, J. The effects of different initial Lactobacillus plantarum concentrations on some properties of fermented carrot juice. J. Food Process. Preserv. 2006, 30, 352–363. [Google Scholar] [CrossRef]
- Di Cagno, R.; Coda, R.; de Angelis, M.; Gobbetti, M. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol. 2013, 33, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Doron, S.I.; Hibberd, P.L.; Gorbach, S.L. Probiotics for prevention of antibiotic-associated diarrhea. J. Clin. Gastroenterol. 2008, 42, 58–63. [Google Scholar] [CrossRef] [PubMed]
- Grin, P.M.; Kowalewska, P.M.; Alhazzan, W.; Fox-Robichaud, A.E. Lactobacillus for preventing recurrent urinary tract infections in women: Meta-analysis. Can. J. Urol. 2013, 20, 6607–6614. [Google Scholar] [PubMed]
- Dylag, K.; Hubalewska-Mazgaj, M.; Surmiak, M.; Szmyd, J.; Brzozowski, T. Probiotics in the mechanism of protection against gut inflammation and therapy of gastrointestinal disorders. Curr. Pharm. Des. 2014, 20, 1149–1155. [Google Scholar] [CrossRef] [PubMed]
- Tomaro-Duchesneau, C.; Saha, S.; Malhotra, M.; Jones, M.L.; Labbe, A.; Rodes, L.; Kahouli, I.; Prakash, S. Effect of orally administered L. fermentum NCIMB 5221 on markers of metabolic syndrome: An in vivo analysis using ZDF rats. Appl. Microbiol. Biotechnol. 2014, 98, 115–126. [Google Scholar] [CrossRef] [PubMed]
- Sivamaruthi, B.S. A comprehensive review on clinical outcome of probiotic and synbiotic therapy for inflammatory bowel diseases. Asian Pac. J. Trop. Biomed. 2018, 8, 179–186. [Google Scholar] [CrossRef]
- Bansal, S.; Singh, A.; Mangal, M.; Sharma, S.K. Isolation and characterization of lactic acid bacteria from fermented Foods. Vegetos 2013, 26, 325–330. [Google Scholar] [CrossRef]
- Ho, J.C.K.; Sze, LY. Isolation, identification and characterization of enzyme-producing lactic acid bacteria from traditional fermented foods. Biosci. Horiz. 2018, 11, hzy004. [Google Scholar] [CrossRef]
- Linh, N.T.H.; Sakai, K.; Taoka, Y. Screening of lactic acid bacteria isolated from fermented food as potential probiotics for aquacultured carp and amberjack. Fish. Sci. 2018, 84, 101–111. [Google Scholar] [CrossRef]
- Ostergaard, A.; Embarek, P.K.B.; Wedell-Neergaard, C.; Huss, H.H.; Gram, L. Characterization of anti-listerial lactic acid bacteria isolated from Thai fermented fish products. Food Microbiol. 1998, 15, 223–233. [Google Scholar] [CrossRef]
- Rattanachaikunsopon, P.; Phumkhachorn, P. Isolation and preliminary characterization of a bacteriocin produced by Lactobacillus plantarum N014 isolated from Nham, a traditional Thai fermented pork. J. Food Prot. 2006, 69, 1937–1943. [Google Scholar] [CrossRef] [PubMed]
- Srionnual, S.; Yanagida, F.; Lin, L.; Hsiao, K.; Chen, Y. Weissellicin 110, a newly discovered bacteriocin from Weissella cibaria 110, isolated from Plaa-Som, a fermented fish product from Thailand. Appl. Environ. Microbiol. 2007, 73, 2247–2250. [Google Scholar] [CrossRef] [PubMed]
- Woraprayote, W.; Pumpuang, L.; Tosukhowong, A.; Roytrakul, S.; Perez, R.H.; Zendo, T.; Sonomoto, K.; Benjakul, S.; Visessanguan, W. Two putatively novel bacteriocins active against Gram-negative food borne pathogens produced by Weissella hellenica BCC 7293. Food Control 2015, 55, 176–184. [Google Scholar] [CrossRef]
- Prachyakij, P.; Schnurer, J.; Charernjiratrakul, W.; Kantachote, D. Selection and identification of lactic acid bacteria that inhibit yeast contaminants isolated from fermented plant beverages. Songklanakarin J. Sci. Technol. 2007, 29, 211–218. [Google Scholar]
- Wilaipun, P.; Zendo, T.; Okuda, K.; Nakayama, J.; Sonomoto, K. Identification of the Nukacin KQU-131, a new type-A(II) lantibiotic produced by Staphylococcus hominis KQU-131 isolated from Thai fermented fish product (Pla-ra). Biosci. Biotechnol. Biochem. 2008, 72, 2232–2235. [Google Scholar] [CrossRef] [PubMed]
- Petchkongkaew, A.; Taillandier, P.; Gasaluck, P.; Lebrihi, A. Isolation of Bacillus spp. from Thai fermented soybean (Thua-nao): Screening for aflatoxin B1 and ochratoxin A detoxification. J. Appl. Microbiol. 2008, 104, 1495–1502. [Google Scholar] [CrossRef] [PubMed]
- Charernjiratragul, W.; Bhoopong, P.; Kantachote, D.; Jomduang, S.; Kong-Ngoen, R.; Nair, G.B.; Vuddhakul, V. Inhibitory activity of lactic acid bacteria isolated from Thai fermented food against pandemic strains of Vibrio parahaemolyticus. J. Food Saf. 2010, 30, 67–82. [Google Scholar] [CrossRef]
- Leelavatcharamas, V.; Arbsuwan, N.; Apiraksakorn, J.; Laopaiboon, P.; Kishida, M. Thermotolerant bacteriocin-producing lactic acid bacteria isolated from Thai local fermented foods and their bacteriocin productivity. Biocontrol Sci. 2011, 16, 33–40. [Google Scholar] [CrossRef] [PubMed]
- Saelao, S.; Maneerat, S.; Kaewsuwan, S.; Rabesona, H.; Choiset, Y.; Haertle, T.; Chobert, J.M. Inhibition of Staphylococcus aureus in vitro by bacteriocinogenic Lactococcus lactis KTH0-1S isolated from Thai fermented shrimp (Kung-som) and safety evaluation. Arch. Microbiol. 2017, 199, 551–562. [Google Scholar] [CrossRef] [PubMed]
- Noonpakdee, W.; Santivarangkna, C.; Jumriangrit, P.; Sonomoto, K.; Panyim, S. Isolation of nisin-producing Lactococcus lactis WNC 20 strain from nham, a traditional Thai fermented sausage. Int. J. Food Microbiol. 2003, 81, 137–145. [Google Scholar] [CrossRef]
- Tasaku, S.; Siripornadulsil, S.; Siripornadulsil, W. Inhibitory activity of food-originated Pediococcus pentosaceus NP6 against Salmonella enterica serovar Typhimurium in Nile Tilapia by-products. Chiang Mai J. Sci. 2017, 44, 383–393. [Google Scholar]
- Phromraksa, P.; Nagano, H.; Boonmars, T.; Kamboonruang, C. Identification of proteolytic bacteria from Thai traditional fermented foods and their allergenic reducing potentials. J. Food Sci. 2008, 73, M189–M195. [Google Scholar] [CrossRef] [PubMed]
- Phoottosavako, M.; Keeratipibul, S.; Techo, S.; Tanasupawat, S. Identification and characterization of lipolytic bacteria from Thai fermented foods. Malays. J. Microbiol. 2015, 11, 231–239. [Google Scholar] [CrossRef]
- Klayraung, S.; Viernstein, H.; Sirithunyalug, J.; Okonogi, S. Probiotic properties of Lactobacilli isolated from Thai traditional food. Sci. Pharm. 2008, 76, 485–503. [Google Scholar] [CrossRef]
- Meidong, R.; Doolgindachbaporn, S.; Jamjan, W.; Sakai, K.; Tashiro, Y.; Okugawa, Y.; Tongpim, S. A novel probiotic Bacillus siamensis B44v isolated from Thai pickled vegetables (Phak-dong) for potential use as a feed supplement in aquaculture. J. Gen. Appl. Microbiol. 2017, 63, 246–253. [Google Scholar] [CrossRef] [PubMed]
- Meidong, R.; Doolgindachbaporn, S.; Sakai, K.; Tongpim, S. Isolation and selection of lactic acid bacteria from Thai indigenous fermented foods for use as probiotics in tilapia fish Oreochromis niloticus. AACL Bioflux 2017, 10, 455–463. [Google Scholar]
- Chunhachart, O.; Itoh, T.; Sukchotiratana, M.; Tanimoto, H.; Tahara, Y. Characterization of γ-glutamyl hydrolase produced by Bacillus sp. isolated from Thai thua-nao. Biosci. Biotechnol. Biochem. 2006, 70, 2779–2782. [Google Scholar] [CrossRef] [PubMed]
- Nanasombat, S.; Treebavonkusol, P.; Kittisrisopit, S.; Jaichalad, T.; Phunpruch, S.; Kootmas, A.; Nualsri, I. Lactic acid bacteria isolated from raw and fermented pork products: Identification and characterization of catalase producing Pediococcus pentosaceus. Food Sci. Biotechnol. 2017, 26, 173–179. [Google Scholar] [CrossRef]
- Sirilun, S.; Chaiyasut, C.; Kantachote, D.; Luxananil, P. Functional properties of β-glucosidase-producing Lactobacillus plantarum SC 359 isolated from Thai fermented soybean food. Acta Aliment. 2012, 41, 451–464. [Google Scholar] [CrossRef]
- Woraharn, S.; Lailerd, N.; Sivamaruthi, B.S.; Wangcharoen, W.; Sirisattha, S.; Chaiyasut, C. Screening and kinetics of glutaminase and glutamate decarboxylase producing lactic acid bacteria from fermented Thai foods. Food Sci. Technol. 2014, 34, 793–799. [Google Scholar] [CrossRef] [Green Version]
- Toyokawa, Y.; Takahara, H.; Reungsang, A.; Fukuta, M.; Hachimine, Y.; Tachibana, S.; Yasuda, M. Purification and characterization of a halotolerant serine proteinase from thermotolerant Bacillus licheniformis RKK-04 isolated from Thai fish sauce. Appl. Microbiol. Biotechnol. 2010, 86, 1867–1875. [Google Scholar] [CrossRef] [PubMed]
- Ratanaburee, A.; Kantachote, D.; Charernjiratrakul, W.; Sukhoom, A. Selection of c-aminobutyric acid-producing lactic acid bacteria and their potential as probiotics for use as starter cultures in Thai fermented sausages (Nham). Int. J. Food Sci. Technol. 2013, 48, 1371–1382. [Google Scholar] [CrossRef]
- Sanchart, C.; Rattanaporn, O.; Haltrich, D.; Phukpattaranont, P.; Maneerat, S. Lactobacillus futsaii CS3, a new GABA-producing strain isolated from Thai fermented shrimp (Kung-Som). Indian J. Microbiol. 2017, 57, 211–217. [Google Scholar] [CrossRef] [PubMed]
- Smitinont, T.; Tansakul, C.; Tanasupawat, S.; Keeratipibul, S.; Navarini, L.; Bosco, M.; Cescutti, P. Exopolysaccharide-producing lactic acid bacteria strains from traditional Thai fermented foods: Isolation, identification and exopolysaccharide characterization. Int. J. Food Microbiol. 1999, 51, 105–111. [Google Scholar] [CrossRef]
- Woraharn, S.; Lailerd, N.; Sivamaruthi, B.S.; Wangcharoen, W.; Peerajan, S.; Sirisattha, S.; Chaiyasut, C. Development of fermented Hericium erinaceus juice with high content of l-glutamine and l-glutamic acid. Int. J. Food Sci. Technol. 2015, 50, 2104–2112. [Google Scholar] [CrossRef]
- Chaiyasut, C.; Woraharn, S.; Sivamaruthi, B.S.; Kesika, P.; Lailerd, N.; Peerajan, S. Lactobacillus fermentum HP3 mediated fermented Hericium erinaceus juice as a health promoting food supplement to manage diabetes mellitus. J. Evid. Based Integr. Med. 2018, 23, 1–9. [Google Scholar] [CrossRef] [PubMed]
S. No. | Source | Name of the Isolate | Bioactivity | Other Observations | Ref. |
---|---|---|---|---|---|
1 | Fermented fish | Lactobacillus spp. | Anti-listerial activity | Displayed antimicrobial activity against Vibrio cholerae, V. parahaemolyticus, Aeromonas sp. | [24] |
2 | Fermented pork (Nham) | L. plantarum N014 | Anti-listerial activity, Bacteriocin production | Displayed antimicrobial activity against several Gram-positive and Gram-negative microbes. | [25] |
3 | Fermented fish (Plaa-Som) | Weissella cibaria 110 | Bacteriocin production | The bacteriocin, weissellicin 110, was active against some Gram-positive bacteria. Peptide mass was 3487.8 Da. | [26] |
4 | Fermented pork meat (Nham) | Weissella hellenica BCC 7293 | Bacteriocin production (7293A and 7293B) | Active against Gram-negative foodborne pathogens. | [27] |
5 | Fermented foods | L. plantarum | Anti-yeast activity | The isolated strains were tested against Rhodotorula spp., which were isolated from contaminated fermented plant beverages | [28] |
6 | Fermented fish (Pla-ra) | Staphylococcus hominis KQU-131 | Bacteriocin production | Nukacin-KQU-131, a new variant of nukacin ISK-1, was identified. | [29] |
7 | Fermented soybean (Thua-nao) | Bacillus spp. | Anti-Aspergillus activity | The isolate inhibited the growth of Aspergillus flavus and A. westerdijkiae, and detoxified aflatoxin B1 and ochratoxin A. | [30] |
8 | Fermented pork | L. plantarum (PSU-LAB71) | Inhibits V. parahaemolyticus, and V. cholerae | The isolate PSU-LAB71 was active against pandemic strains of Vibrio and found as a probiotic. | [31] |
9 | Fermented foods | Pediococcus acidilactici | Active against Gram-positive bacteria | P. acidilactici produced heat-tolerant bacteriocin. | [32] |
10 | Fermented shrimp(Kung-som) | Lactococcus lactis KTH0-1S | Anti-Staphylococcus aureus activity | Bacteriocin production (Nisin Z). The isolate KTH0-1S was safe and could be used to protect fermented seafood. | [33] |
11 | Fermented pork meat (Nham) | L. lactis WNC 20 | Active against foodborne pathogens | Heat-stable bacteriocin production (Nisin Z like). | [34] |
12 | Fermented fish (Nam-Pla) | P. pentosaceus NP6 | Anti-Salmonella enterica serovar Typhimurium activity | Active against both Gram-positive and Gram-negative pathogens. The isolate NP6 exhibited some probiotic properties. | [35] |
Source | Name of the Isolate | Bioactivity | Other Observations | Ref. |
---|---|---|---|---|
Lytic Activity | ||||
Fermented soybean (Thua Nao), fermented rice-noodle (Kha Nhom Jeen) | Bacillus subtilis, B. licheniformis | Proteolytic activity | The crude extract of culture supernatant showed in vitro anti-allergic activity. | [36] |
Fermented meat and seafood | Bacillus spp. Paenibacillus spp. | Lipolytic activity | [37] | |
Probiotic Strains | ||||
Fermented pork, and tea leaves, | Lactobacillus fermentum | Probiotic | Strains were sensitive to some antibiotics and active against Escherichia coli, Salmonella Typhi, and Staphylococcus aureus. | [38] |
Thai pickled vegetables (Phak-dong) | B. siamensis B44v | Probiotic in hybrid catfish culture | Bacteriocin production and activity against Gram-positive and Gram-negative pathogens. Sensitive to tested antibiotics. Protected the hybrid catfish from Aeromonas hydrophila FW52 infection. | [39] |
Thai indigenous fermented foods | L. plantarum CR1T5 | Probiotic in tilapia fish culture | Activity against fish pathogens (Aeromonas caviae, A. hydrophila, and Streptococcus agalactiae). The supplementation of CR1T5 enhanced the survivability of infected fish, and also enhanced the growth. | [40] |
Enzyme Production | ||||
Fermented soybean (Thua-nao) | Bacillus spp. | γ-Glutamyl hydrolase production | The enzyme was about 28 kDa. The enzyme acted on the γ-glutamyl linkage of γ-polyglutamic acid. | [41] |
Fermented pork | Pediococcus pentosaceus | Catalase production | Activity against S. Typhimurium. Hematin enhanced the catalase production, but was not necessary for production (i.e., heme-independent catalase). | [42] |
Fermented soybean | L. plantarum SC359 | β-glucosidase production | Activity against representative microbial pathogens. The strain competed for pathogenic adherence to Caco-2 cells. | [43] |
Many fermented foods | L. brevis, and L. fermentum | Glutaminase and glutamate decarboxylase production | The optimal conditions for the enzyme production were found at pH 6.5, temperature 40 °C, and 10 days of incubation time. | [44] |
Fish sauce | Bacillus licheniformis RKK-04 | Serine proteinase production | Thermotolerant subtilisin-like alkaline serine proteinase enzyme. pH 10.0 and 50 °C as optimal conditions for enzyme production. The enzyme from RKK-04 could be used in fish sauce fermentation. | [45] |
Gamma-Aminobutyric Acid Production | ||||
Many fermented foods | L. namurensis, P. pentosaceus | γ-Aminobutyric acid (GABA) production | Four isolates were isolated and found to produce GABA (7339–9060 mg/L) in the culture medium. Two isolates (HN8 and NH2) were recommended for use in fermented pork as a starter culture. | [46] |
Fermented shrimp (Kung-Som) | L. futsaii CS3 | GABA production | Reported primary GABA producer, and had the ability to convert 99% monosodium glutamate to GABA. | [47] |
Exopolysaccharide Production | ||||
Many fermented foods | P. pentosaceus (AP-1, and AP-3) | Exopolysaccharide Production | Dextran class of exopolysaccharide. | [48] |
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Sivamaruthi, B.S.; Kesika, P.; Chaiyasut, C. Thai Fermented Foods as a Versatile Source of Bioactive Microorganisms—A Comprehensive Review. Sci. Pharm. 2018, 86, 37. https://doi.org/10.3390/scipharm86030037
Sivamaruthi BS, Kesika P, Chaiyasut C. Thai Fermented Foods as a Versatile Source of Bioactive Microorganisms—A Comprehensive Review. Scientia Pharmaceutica. 2018; 86(3):37. https://doi.org/10.3390/scipharm86030037
Chicago/Turabian StyleSivamaruthi, Bhagavathi Sundaram, Periyanaina Kesika, and Chaiyavat Chaiyasut. 2018. "Thai Fermented Foods as a Versatile Source of Bioactive Microorganisms—A Comprehensive Review" Scientia Pharmaceutica 86, no. 3: 37. https://doi.org/10.3390/scipharm86030037
APA StyleSivamaruthi, B. S., Kesika, P., & Chaiyasut, C. (2018). Thai Fermented Foods as a Versatile Source of Bioactive Microorganisms—A Comprehensive Review. Scientia Pharmaceutica, 86(3), 37. https://doi.org/10.3390/scipharm86030037