Importance of lactic acid bacteria in Asian fermented foods
© Rhee et al; licensee BioMed Central Ltd. 2011
Published: 30 August 2011
Lactic acid bacteria play important roles in various fermented foods in Asia. Besides being the main component in kimchi and other fermented foods, they are used to preserve edible food materials through fermentation of other raw-materials such as rice wine/beer, rice cakes, and fish by producing organic acids to control putrefactive microorganisms and pathogens. These bacteria also provide a selective environment favoring fermentative microorganisms and produce desirable flavors in various fermented foods. This paper discusses the role of lactic acid bacteria in various non-dairy fermented food products in Asia and their nutritional and physiological functions in the Asian diet.
Fermentation is one of the oldest forms of food preservation in the world. Fermented dairy products and their microbial and functional characteristics have been widely studied. Most East-Asian fermented foods are non-dairy products featuring various other food raw-materials such as cereals, soybeans, fruits, and vegetables, as well as fish and other marine products. The importance of lactic acid bacteria in fermented non-dairy foods and beverages was reviewed previously in the early 1990s in an overview of the role of lactic acid bacteria in kimchi, fermented fish products and vegetable yogurts . The role of lactic acid bacteria in rice wine/beer fermentation has also been reported . Steamed bread such as idli from India and puto from the Philippines, which are made with rice, are fermented by Leuconostoc. Korean sikhae and Philippine burong isda/dalag, which are made by mixing salted fish and cereals, are also fermented in early stages by Leuconostoc mesenteroides[3, 4]. L. mesenteroides initiates relatively rapid growth in various plant materials (vegetables and cereals) over a wide range of temperatures and salt concentrations in comparison with other lactic acid bacteria. During growth, L. mesenteroides produces carbon dioxide and acids, leading to modification of the environment as well as conditions that favor the growth of other lactic acid bacteria. Analogously, the various fermentation pathways initiated by L. mesenteroides include prominent roles for other lactic acid bacteria belonging to the genera Lactobacillus and Pediococcus at later stages.
The numerous fermented food products in Asia can be categorized into five groups: (1) fermented soybean products, (2) fermented fish products, (3) fermented vegetable products, (4) fermented bread and porridges, and (5) alcoholic beverages. Lactic acid bacteria are involved in all of these fermentations to a varying extent, having either positive or negative effects on the eventual product. In making soybean sauce and paste, souring is indicative of poor fermentation and should be avoided. It is caused by undesirable yeast contamination, which is related to the fact that soybeans are not favorable substrates for the growth of lactic acid bacteria. In the case of alcoholic fermentation, lactic acid bacteria generally deteriorate the quality of the products. However, in traditional cereal alcoholic fermentation, lactic acid bacteria during the initial stage of fermentation provide a favorable environment for later stage fermentations including alcohol production, thereby contributing to the characteristic taste and aroma of the beverage. In fermentation of vegetable-derived raw materials, lactic acid bacteria play a major role, and the optimum amount of acid production varies with the product type .
The advantages of acidic food fermentation are: (1) renders foods resistant to microbial spoilage and the development of food toxins, (2) makes foods less likely to transfer pathogenic microorganisms, (3) generally preserves foods between the time of harvest and consumption, (4) modifies the flavor of the original ingredients and often improves nutritional value .
Examples of acid-fermented foods in Asia
Lactic acid bacteria
rice, glutinous rice
Mucor, Rhizopus, Aspergilus
Sour, sweet liquid, paste
Mucor indicus, Candida
Dark brown liquid sour alcoholic
Thailand, Korea, Japan
Korean cabbage, radish, various vegetables, salt
salad, side dish
salad, side dish
salad, salt side dish
salad, side dish
Fermented fish and meat
sea water fish
cooked millet, salt
sea water fish
cooked millet, salt
fresh water fish rice,
fresh water fish salt,
shrimp, rice, salt
pork, galic, salt, rice
pork meat in banana leaves
pork, salt, cooked rice
Rice-wine is a generic name referring to alcoholic beverages made from cereals, mainly rice, in East-Asia. Traditional alcoholic beverages vary from crystal-clear products to turbid liquid or thick gruels and pastes. Clear products, which are generally called shaosingjiu in China, cheongju in Korea, and sake in Japan, contain around 15% alcohol and are designated as rice-wine, whereas turbid beverages, takju (or maggolli) in Korea and tapuy in the Philippines, contain less than 8% alcohol along with suspended insoluble solids and live yeasts, and are referred to as rice-beer .
The process of cereal alcohol fermentation involves a two-step fermentation; solid state fermentation wherein molds grow on raw or cooked cereals, which is called nuruk, followed by mashing the nuruk with additional cereals to produce alcohol by yeast. The dried and powdered nuruk is then mixed with water and stored in a cool place for several days to make the mother brew. During this period, microbial amylases and proteases are produced, which convert the starch present in the cereal raw-materials into sugars. The acid-forming bacteria in nuruk then produce organic acids, reducing the pH to below 4.5, which favors the growth of yeast at the later stage of alcohol fermentation. About two to three volumes of cooked grains and water are then added to the mother brew to prepare the first fermentation mash. Upon addition of new cooked grains and water to the mash, the production volume increases while the alcohol concentration and quality of the final product are enhanced. Multiple brews prepared by adding two to nine additions of newly cooked grains to the fermenting mash have been described in the old literatures .
Changes in concentrations of microorganisms during samhaeju and cheongju brewing.
Japanese style cheongju
4.2 x 10 5
< 10 2
9.8 x 10 4
< 10 2
3.9 x 10 5
< 10 2
Acid forming bacteria
3.1 x 10 5
8.9 x 10 7
8.6 x 10 4
< 10 2
7.5 x 10 6
3.3 x 10 6
6.3 x 10 4
< 10 2
3.3 x 10 5
8.5 x 10 7
7.5 x 10 4
< 10 2
< 10 2
1.8 x 10 6
1.8 x 10 6
3.2 x10 7
2 x 10 6
< 10 2
2.4 x 10 6
1.6 x 10 6
1.9 x 10 7
2.5 x 10 7
< 10 2
4.6 x 10 6
1.4 x 10 6
2.6 x10 6
3.1 x 10 6
Acid-fermented bread and noodle
Lactic acid fermentation of bread dough improves the keeping quality and flavor of the baked products. It also enhances the palatability of bread made from low grade flours and under-utilized cereals. Acid-fermented breads and pancakes are an important staple food for people in Africa and some parts of Europe and Asia .
L. mesenteroides and Streptococcus faecalis are developed concomitantly with soaking and then continue to multiply following grinding. Both genera eventually reach higher than 1x109 cells/gram of the finished batter . L. mesenteroides is considered to be essential for leavening of the batter, and it is also considered to be responsible for acid production in idli, dosa, and related products, together with S. faecalis.
These organisms appear to be present in the raw-material ingredients, and therefore it is generally not required to add them as inoculum. Aerobic contaminants that are usually present in the raw-materials are eliminated partly by careful washing of the ingredients and partly by the acidic conditions generated by the fermentation. However, Batra and Millner  isolated Torulopsis candida and Trichosporon pulluans from idli batter and prepared authentic idli only by the joint action of both yeasts in the mixture. Both T. pullulans and T. candida provide characteristic acidity, whereas T. candida also produces gas during fermentation.
Kichuddok is prepared at the household level and consumed less frequently at special occasions in Korea, whereas puto is normally consumed as a breakfast and snack in the Philippines. Puto is a common food for the lower-income group, but special types with added cheese, eggs, etc., are consumed as delicacies by the higher-income group. In a number of Philippine towns, preparation of puto is an important cottage industry .
Thai rice-noodle, khanom-jeen, is also made from acid-fermented rice . Soaked rice is drained and fermented for at least 3 days before grinding, and Lactobacillus species and Streptococcus species are involved in the acid fermentation. Acid-fermented porridges, such as ogi and uji in African countries, are not common in the Asia-Pacific region.
Most Asian countries produce mungbean starch, and mungbean starch noodles are dietary staples of the Chinese. The process for manufacturing mungbean starch involves acidic bacterial fermentation, in which the mungbeans are hydrated by soaking in water inoculated with 12-hr steep water from a previous fermentation to ensure acidification. The principal microorganisms found in the steep water are L. mensenteroides, Lactobacillus casei, Lactobacillus cellobiosus, and Lactobacillus fermentum. Lactic acid fermentation, which reduces the pH from 6.0 to about 4.0 protects the starch granules from spoilage and putrefaction that would otherwise occur in non-inoculated ground bean slurries .
Acid-fermented fish and meat
Acid-fermented vegetables are important sources of vitamins and minerals. L. mesenteroides has been found to be important in the initiation of fermentation of many vegetables, i.e. cabbages, beets, turnips, cauliflower, green beens, sliced green tomatoes, cucumber, olives, and sugar beet silages. In vegetables, L. mesenteroides grows rapidly and produces carbon dioxide and acids that quickly lower the pH, thereby inhibiting the development of undesirable microorganisms and the activity of their enzymes as well as preventing unfavorable softening of the vegetables. The carbon dioxide produced replaces air and provides anaerobic conditions that favor stabilization of ascorbic acid and the natural colors of the vegetables. L. mesenteroides converts glucose to approximately 45% levorotatory D-lactic acid, 25% carbon dioxide, and 25% acetic acid and ethyl alcohol. Moreover, fructose is partially reduced to mannitol, which subsequently undergoes secondary fermentation (see below) to yield equimolar quantities of lactic acid and acetic acid. The combination of acids and alcohol are conducive to the formation of esters, which impart desirable flavors . Overall, the initial growth of L. mesenteroides leads to modification of the environment that favors the growth of other lactic acid bacteria. Secondary fermentation in these processes, especially by homofermentative Lactobacillus species, leads to further reduction of the pH and ultimately growth of L. mesenteroides.
Kimchi fermentation is the Korean method of preserving the fresh and crispy texture of vegetables during the winter when fresh vegetables are not available. Almost all kinds of vegetables can be made into kimchi; cabbages, radish, cucumber, Welsh onion leaves, and mustard leaves are the popular main ingredients. The name of each particular kimchi is based on the main ingredients: cabbage kimchi (baechukimchi), radish kimchi, cucumber kimchi, etc. Minor ingredients such as garlic, red pepper, green onion, ginger, and salt are also added. Fermented fish products and other seasoning agents are optional. kimchi has a sour, sweet, and carbonated taste and is usually served cold . It is a side dish that is commonly served with cooked rice and soup.
The dominant species of Lactobacillus in the later stages of kimchi fermentation vary according to the fermentation temperature; Lb. plantarum and Lactobacillus brevis dominate fermentations carried out at 20-30 while Lactobacillus maltaromicus and Lactobacillus bavaricus dominate at 5-7. Lb. plantarum is homofermentative and is the highest acid-producing species of this group, yielding three or four times higher DL-lactic acid content than Leuconostoc species . Low temperature is preferred for kimchi fermentation to prevent the production of high amounts of lactic acid and over-ripening as well as to extend the period of optimum taste.
Recently, the genome probing DNA chip (GPM) method was applied to identify and monitor microbial behavior during fermentation. Over 100 species of microorganisms were identified in kimchi fermentation . Among these, Weisella confuse, Leuconostoc citreum, Lactobacillus curvatus, Lactobacillus sakai, and Lb. fermentum were identified as the important microorganisms.
Changes in concentrations of intestinal pathogens in kimchi during fermentation at 20°C ((CFU/mL)).
Lactic acid bacteria
Several strains of microorganisms that produce bacteriocin have been isolated from kimchi. Enterococcus faecium in kimchi has a broad spectrum of bacteriocin activities, and several Lactobacillus species have been shown to produce anti-microbial compounds [17, 7]. As an example, a heat- and pH-stable bacteriocin, kimchicin GJ7, produced by L. citreum GJ7 was isolated. Notably, the presence of a bacteriocin-sensitive strain, Lb. plantarum, was shown to act as an environmental stimulus to activate the production of kimchicin GJ7 by L. citreum. Furthermore, improved quality and shelf-life of kimchi by fermentation using an induced bacteriocin-producing strain as a starter were previously observed . Recently, a new antifungal compound, 3,6-bis(2-methylpropyl)-2,5-piperazinedion (molecular mass of 226 kDa), was identified as being produced by a Lb. plantarum strain obtained from kimchi, illustrating that the anti-microbial pallet produced during kimchi fermentation may exceed the anti-bacterial activities. Overall, the combination of organic acids and anti-microbial compounds produced during fermentation and the anti-microbial activity of the ingredients regulate the microbiota found in kimchi, and it controls the growth of pathogenic microorganisms without costly treatments and packaging.
The physiological effects of kimchi ingredients and their metabolites have been studied extensively [20, 7]. The anti-tumor activities of cabbage and garlic have been reported by many investigators , whereas extracts of red pepper powder have been shown to exert inhibitory effects against aflatoxin B1-mediated mutagenesis. Additionally, kimchi contains sufficient concentrations of fiber to prevent constipation and colon cancer, as well as exerting prebiotic effects. Finally, the probiotic effect of lactic acid bacteria in kimchi (grown to 108/mL) may assist in digestive and intestinal functions  (Table 4).
Biologically active compounds in kimchi.
reducing the cholesterol level
secretion of neuropeptides
Lactic acid bacteria
L-(+) lactic acid
modulation of T-cell function
Adaptation of lactic acid bacteria in human food cycle
The bacteria isolated from kimchi are identified in Bergey's Manual, but their physiological characteristics seldom match exactly with those characterized in the Manual. L. mesenteroides and Lb. barvaricus isolated from kimchi show many discrepancies in sugar fermentation and vitamin requirements. All Leuconostoc species isolated from kimchi can grow at pH levels below 4.8 as well as in media containing 7% ethanol or 6.5% NaCl . An interesting observation is that L. mesenteroides subspecies show tolerance in artificial digestive fluid at pH 3.0 and also grow in media containing 10% or 40% bile . These properties are similar to those of intestinal microorganisms, such as Lactobacillus acidophilus and Lb. casei, as well as faecal microbial strains. These observations suggest that the major microorganisms in kimchi have adapted to the special environment of Korea as a part of the food cycle from the soil to vegetables, to kimchi, and then to the human intestine, faeces, and the soil again. Adaptations of microorganisms to special environmental conditions have been reported in other fermented foods, i.e. L. mesenteroides in cane juice, Leuconostoc. oenos in grape juice, Pediococcus. halophilus in soy sauce, and the above-mentioned L. mesenteroides in sikhae.
Lactic acid bacteria play important roles in many Asian fermented foods, especially in non-dairy fermented vegetable products. The probiotic functions of lactic acid bacteria in non-dairy fermented foods in Asia have not been fully investigated. L. mesenteroides present in kimchi, for example, probably have probiotic effects. In fact, Koreans who travel overseas for several days without kimchi often experience uncomfortable stomach symptoms and poor digestion. More research is needed to identify the lactic acid bacteria in Asian fermented foods and their physiological functions in the human diet.
The authors deeply appreciate the valuable comments and editorial assistance of Prof. Michiel Kleerebezem, NIZO food research and Wageningen University, The Netherlands.
This article has been published as part of Microbial Cell Factories Volume 10 Supplement 1, 2011: Proceedings of the 10th Symposium on Lactic Acid Bacterium. The full contents of the supplement are available online at http://www.microbialcellfactories.com/supplements/10/S1.
- Lee CH: Importance of lactic acid bacteria in non-dairy food fermentation, in Lactic Acid Fermentation of Non-dairy Food and Beverages. Edited by: Lee, C.H., Adler-Nissen, J. and Barwald, G. 1994, HarnLimWonGoogle Scholar
- Rhee SJ, Lee CYJ, Kim KK, Lee CH: Comparison of the traditional (samhaeju) and industrial (Congju) rice wine brewing in Korea. Korean J. Food Sci. Technol. 2003, 12: 242-247.Google Scholar
- Lee CH, Cho TS, Lim MH, Kang Jh, Yang HC: Studies on the Sik-hae fermentation made by flat-fish. Korean J. Appl. Microbiol. Bioeng. 1983, 11: 53-58.Google Scholar
- Orillo CA, Pederson CS: Lactic acid bacterial fermentation of Burong dalag. Appl. Microbiol. 1968, 16: 1669-1671.Google Scholar
- Lee CH: Food biotechnology. Food Science and Technology. Edited by: Campbell-Platt, G., Wiley-Blackwell. 2009, 85-113.Google Scholar
- Steinkraus KH: Handbook of Indigenous Fermented Foods. 1988, Marcel Dekker, New YorkGoogle Scholar
- Lee CH: Fermentation Technology in Korea. 2001, Korea University PressGoogle Scholar
- Lee CH, Adler-Nissen J, Barwald G: . Lactic Acid Fermentation of Non-dairy Food and Beverages. 1994, HarnLimWonGoogle Scholar
- Mukherjee SK, Albury MN, Pederson CS, Van Veen AG, Steinkraus KH: Role of Leuconostoc mesenteroides in leavening the batter of idle, a fermented food of India. Appl. Microbiol. 1965, 13: 227-231.Google Scholar
- Batra LR, Millner PD: Some Asian fermented foods and beverages and associated fungi. Mycologia. 1974, 66: 942-950. 10.2307/3758313.View ArticleGoogle Scholar
- Rosanaphaiboon T: Khanom-jeen: Traditional food and processing in Asia. Edited by: F. Yanagida, Y. Takai, S. Homa, S. Kato and Y. 1987, Ando. NODAI Research Institute, Tokyo, 48-Google Scholar
- Jamias-Apilado RB, Mabesa RC: Influence of rice and salt on the rate of rice-fish fermentation. The Philippine J. of Biotechnol. 1991, 1: 160-Google Scholar
- Lee CH: Fish fermentation technology. Korean J. Appl. Microbiol. Bioeng. 1989, 17: 645-654.Google Scholar
- Souane M, Kim YB, Lee CH: Microbial characterization of Gajami-sikhae fermentation. Korean J. Appl. Microbial. Bioeng. 1987, 15: 150-157.Google Scholar
- Lee CH: Lactic acid fermented foods and their benefits in Asia. Food Control. 1997, 9: 259-269.View ArticleGoogle Scholar
- Park HY, Bae JW, Lee IS, Kim HI, Lee JS, Ryu BH, Chang YH, Yoon JH, Nam YD, Kang KH: Kimchi starter culture and molecular monitoring technology for the production of new functional Kimchi. Korean Kimchi and Fermentation Technology, Proceedings of Korean Society of Microbiology and Biotechnology Symposium. 2005, Seoul, 49-53.Google Scholar
- Ha DM: Suppression of acidic deterioration of Kimchi during the fermentation process. The Science of Kimchi, Proceedings of the Korean Society of Food Science and Technology Symposium. 1994, Seoul, 43-61.Google Scholar
- Chang JY, Chang HC: Improvements in the quality and shelf life of Kimchi by fermentation with the induced bacteriocin-producing strain, Leuconostoc citreum GJ7 as a starter. J. Food Sci. 2010, 75: 103-110.View ArticleGoogle Scholar
- Yang EJ, Chang HC: Purification of a new antifungal compound produced by AF1 isolated from Kimchi. International J. Food Microbiol. 2010, 139: 56-63. 10.1016/j.ijfoodmicro.2010.02.012.View ArticleGoogle Scholar
- Park KY, Choi HS: The anti-mutagenic and anti-carcinogenic activity of Kimchi. The Science of Kimchi, Proceedings of the Korean Society of Food Science and Technology Symposium. 1994, Seoul, 205-225.Google Scholar
- Park KY, Kim SH, Suh MJ, Chung HY: Inhibitory effect of garlic on the mutagenicity in Salmonella assay system and on the growth of HT-29 human colon carcinoma cells. Korean J. Food Sci. Technol. 1991, 23: 370-374.Google Scholar
- Oh YJ, Hwang IJ, Leitzmann C: Nutritional and physiological evaluation of Kimchi. The Science of Kimchi, Proceedings of the Korean Society of Food Science and Technology. 1994, Seoul, 226-246.Google Scholar
- Lee CH: Kimchi, synbiotic food of Korean. Proceedings of Kimchi Symposium. 2007, IFT Annual Meeting, 1-18.Google Scholar
- So MH: Characterization of psychotrophic lactic acid bacteria isolated from Korean Kimchi. 2001, Ph.D. Thesis, Department of Food Technology, Korea University, Seoul, KoreaGoogle Scholar
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