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Keywords:

  • pancakes;
  • bread;
  • amylolytic starters;
  • snacks;
  • beverages;
  • condiments

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

In the Asian region, indigenous fermented foods are important in daily life. In many of these foods, yeasts are predominant and functional during the fermentation. The diversity of foods in which yeasts predominate ranges from leavened bread-like products such as nan and idli, to alcoholic beverages such as rice and palm wines, and condiments such as papads and soy sauce. Although several products are obtained by natural fermentation, the use of traditional starter cultures is widespread. This minireview focuses on the diversity and functionality of yeasts in these products, and on opportunities for research and development.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Indigenous, also referred to as traditional, fermented foods are those popular products that since early history have formed an integral part of the diet and that can be prepared in the household or in cottage industry using relatively simple techniques and equipment. Some of these products have undergone industrial development and are also now manufactured on a large scale (Wood, 1998; Boekhout & Robert, 2003; Hui et al., 2004). Yeasts occur in a wide range of fermented foods, made from ingredients of plant as well as animal origin. This minireview illustrates a selection of fermented products of particular interest because of the predominant yeasts that contribute to their attractive characteristics. When yeasts are abundant, alone or in stable mixed populations with mycelial fungi or with (usually lactic acid) bacteria, they have a significant impact on food quality parameters such as taste, texture, odour and nutritive value. Among the Asian indigenous fermented food products, we examined pancakes and bread, amylolytic fermentation starters, alcoholic snacks and beverages, and condiments. Table 1 illustrates the diversity of ingredients used. Whereas fermentation plays an important role in the home kitchen, several products are presently manufactured on medium or large industrial scale (Steinkraus, 1989). Up-scaling of processes requires control of the operations and of the quality and safety of ingredients and products. In addition, new aspects of functionality are becoming more important for exploitation. Future prospects for research and development will be discussed at the end of this review.

Table 1.    Yeast-based traditional fermented foods and beverages of Asia
Name of the foodCountryMajor IngredientsFunctional MicrofloraFermentation contributes to:References
  1. AAB, acetic acid bacteria; LAB, lactic acid bacteria.

Pancakes and leavened low-salt bread
 IdliIndia, Sri LankaRice and blackgram dalLAB, Saccharomyces cerevisiaeFlavour, texture, nutritional valueSoni & Sandhu (1991)
 DhoklaIndiaRice and BengalgramLAB, Pichia silvicolaFlavour, texture, nutritional valueKanekar & Joshi (1993)
 Nan, kulcha and bhaturaIndia, Pakistan, Afghanistan, IranWheat flourLAB, Saccharomyces cerevisiae and other yeastsTexture, flavourSandhu et al. (1986)
Amylolytic fermentation starters
 RagiIndonesiaRiceAmylomyces rouxii, Hansenula spp., Saccharomycopsis fibuligeraStarch degradation, alcoholic fermentationHesseltine et al. (1988); Saono et al. (1996)
 Murcha/marchaIndia, NepalRiceMucor spp., Rhizopus spp., Pichia burtonii, Saccharomyces cerevisiaeStarch degradation, alcoholic fermentationShrestha et al. (2002); Tsuyoshi et al. (2005)
 Loog-pangThailandRiceSaccharomycopsis fibuligera, Pichiaanomala and other yeastsStarch degradation, alcoholic fermentationLimtong et al. (2002)
Tane kojiJapanRiceAspergillus oryzae, Aspergillus usamiiStarch and protein degrading enzymes for rice wine making 
 MenVietnamRiceAmylomyces rouxii, Saccharomyces cerevisiaeStarch degradation, alcoholic fermentationDung et al. (2005)
Sweet – low alcoholic snacks fermented with amylolytic starters
 Tapé ketan, Tapé ketella/peujeumIndonesiaRice, cassava tubersAmylomyces rouxii, Mucor spp., Rhizopus spp., Saccharomycopsis fibuligera, Pichia burtonii, Pichia anomalaStarch degradation, glucose formation, alcoholic fermentation, flavourKo (1986)
 Kao-markThailandRice  Boon-Long (1986)
Wines brewed with amylolytic starters
 SakéJapanRiceAspergillus oryzae, Saccharomyces sake, Hansenula anomalaSaccharification, alcohol, flavour 
 Yakju and takjuKoreaRice, wheat, barley, maize, milletAspergillus oryzae, Aspergillus sojae, Rhizopus spp., Saccharomyces cerevisiae, Hansenula anomala, Hansenula subpelliculosa, Candida sake, Torulaspora inconspicua, Pichia polymorphaSaccharification, alcohol, flavourRhee et al. (2003)
 TapuyThe PhilippinesRiceSaccharomycopsis fibuligera, Rhodotorula glutinis, Debaryomyces hansenii, Candida parapsilosis, Trichosporon fennicumSaccharification, alcohol, flavourKozaki & Uchimura (1990)
 Ruou nep thanVietnamPurple glutinous riceAmylomyces rouxii, Saccharomyces cerevisiaeSaccharification, alcohol, flavourDung (2004)
 Jnard/jaanr/thumbaNepal, India, BhutanFinger millet/rice/maize/wheatMucor spp., Rhizopus spp., Saccharomycopsis fibuligera, Pichia anomala, Saccharomyces cerevisiae, LABSaccharification, alcohol, flavourTamang et al. (1988)
Beverages fermented from sugary juices
 Palm wines (Toddy/ tari, Tuack, Tuba)India, Bangladesh, Sri Lanka, Thailand, Malaysia, Indonesia, the PhilippinesSap of coconut, date or palmyra palmLAB, AAB, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Kodamaea ohmeri and other yeastsAlcohol and flavour productionBatra & Millner (1974); Joshi et al. (1999)
 Kombucha/tea- fungusJapan, Indonesia, China, RussiaTea liquor and sugarAAB, Brettanomyces spp., Zygosaccharomyces kombuchaensis, Saccharomyces spp.Organic acids, vitamins, health beverageMayser et al. (1995)
Condiments
 WadiIndia, PakistanBlackgram dalCandida krusei, LABAcidification, leavening, nutritional valueSandhu & Soni (1989)
 Papad/papadamIndiaBlackgram dalCandida krusei, Saccharomyces cerevisiaeTexture, flavourShurpalekar (1986)
 Soy saucesJapan, ChinaSoybeans and wheatAspergillus oryzae, Aspergillus sojae, Zygosaccharomyces rouxii, Candida spp.Enzymic degradation of starch and proteins, formation of flavourAidoo et al. (1994)
 MisoJapanRice and soybeansAspergillus oryzae, Zygosaccharomyces rouxii, LABFlavourEbine (1989)

Pancakes and breads

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Pancakes

Idli, dosa and appam, consumed in India and Sri Lanka, are cereal–legume mixture foods which, from a nutritional point of view, are advantageous because of an improved balance of carbohydrates and proteins. To prepare idli, rice (Oryza sativa) and blackgram (Phaseolus mungo) dal (dehusked split seeds) are soaked separately in water. The soaked rice is then coarsely ground, whereas dal is ground to a smooth mucilaginous paste. The two slurries (2 : 1) are mixed with salt, put in a closed container and left overnight to allow a definite leavening (a two- to three-fold increase in the original volume) and to develop a pleasant acid flavour. The fermented batter is poured in cups of an idli pan, and steamed until the idli cakes (Fig. 1a) are soft and spongy with a honeycomb structure inside. A slightly modified version of this batter, where the proportion of rice is increased and both the ingredients are finely ground, is used to prepare two additional foods: dosa (highly seasoned griddled pancake) and appam (poached egg-like pancake).

image

Figure 1.   (a) Idli (centre) served hot, with sambar (left) and chutney (right). (b) Amylolytic fermentation starters: Men (left) and Ragi (right). (c) Condiments: wadis of Punjab (left) and Bengal (top right), showing cavities in some inverted wadis. Middle-sized wadis (bottom right) are made of lentil. (d) Condiments: Papads (top) as marketed, (bottom) baked.

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Idli is a natural fermented food. Both bacteria and yeasts are generally introduced by the two main ingredients and participate in the fermentation. A bit of freshly fermented batter (‘backslop’) is often added to the newly ground batter. As the fermentation progresses, both bacterial and yeast cell numbers increase significantly with a concomitant decrease in pH, and an increased volume of batter, amylase and protease activity. Leuconostoc mesenteroides is the most commonly encountered bacterium (Nout & Sarkar, 1999). During fermentation, along with L. mesenteroides, Saccharomyces cerevisiae, Debaryomyces hansenii, Pichia anomala and Guehomyces pullulans are predominant among the yeasts appearing first, and Trichosporon cutaneum develops subsequently. Eventually, only S. cerevisiae persists (Soni & Sandhu, 1991).

The role of yeasts in idli batter fermentation is controversial. Although the fermentation was reported (Ramakrishnan, 1979) to be entirely due to heterofermentative L. mesenteroides, later work has shown yeast involvement in the fermentation (Venkatasubbaiah et al., 1984). The major functions of the fermentation include the leavening of the batter and the improvement of taste and nutritional value of idli. The role of lactic acid bacteria is to reduce the pH of the batter to an optimum level (pH 4.1–4.5) for yeast activity. Yeasts help in the degradation of starch (which cannot be carried out by L. mesenteroides) into maltose and glucose by producing extracellular amylolytic enzymes. They also produce carbon dioxide and play a significant role in leavening. The sources of the yeast strains are the surface of stone grinders used for preparation of batter, and the rice used in batter preparations. Not only the load but also the diversity of yeasts in fermenting batter is greater in winter than in summer. Fermentation of batter by inoculating the ingredients with individual yeasts and in combination with L. mesenteroides reveals that yeasts contribute not only to gas production, resulting in good texture, but also towards sensory qualities. The higher activity of amylases, levels of B vitamins and free amino acids attained in yeast-enriched fermentations suggest the positive contribution of yeasts to these constituents (Venkatasubbaiah et al., 1984, 1985). It can be said that even if the yeasts are not essential for the leavening of idli batter, they are certainly important for the desirable organoleptic qualities and on nutritional grounds. The possible synergism between bacteria and yeasts remains to be determined.

Dhokla, popular all over India, is similar to idli except that the dal used is of Bengalgram (Cicer arietinum). During fermentation, there is an almost two-fold rise in the batter volume and a drop of pH from 5.2 to 4.5. The microorganisms involved in the fermentation are Lactobacillus fermentum, L. mesenteroides and Pichia silvicola (up to 107 g−1) (Joshi et al., 1989). The lactic acid bacteria contribute lactic acid and acetoin, imparting a sour taste and a pleasant flavour. The yeast produces folic acid and raises the volume of the batter, imparting sponginess to the product (Kanekar & Joshi, 1993).

Breads

Nan (naan) is generally consumed as a staple food by the people of Afghanistan, Iran, India and Pakistan. It is a flat leavened bread, made by mixing white wheat flour with sugar, salt, backslop and water. The dough is left for 12–24 h, formed into balls and flattened. Smoothly flattened dough is slapped onto the inner wall of the clay-clad brick oven, called ‘tandoor’, where it sticks while baking until the dough is puffed-up and light brown.

From a new dough (pH 5.9) for making nan, 105 yeast cfu g−1 and 102 lactic acid bacteria cfu g−1 were obtained, as compared with respective counts of 108 and 109 from ripe, fermented dough (pH 4.8). Saccharomyces cerevisiae is the predominant yeast (Sandhu et al., 1986).

Bhaturas (pathuras) and kulchas of northern India and Pakistan are prepared from similar leavened doughs; they are respectively deep-fried in oil or prepared on a griddle. Kulcha dough contains yeasts and lactic acid bacteria. The yeasts belong mainly to the genera Saccharomyces, Candida, Hansenula, Saccharomycopsis, Kluyveromyces, Rhodotorula, Pichia, Torulopsis, Trichosporon and Debaryomyces (Sandhu et al., 1986).

Amylolytic fermentation starters

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Amylolytic starters are used in the form of starchy tablets containing mixed cultures of starch-degrading moulds and fermenting yeasts. They are used for the manufacture of beers, wines and pasty snacks from various kinds of cereals and starchy crops, such as rice, sorghum, millet and cassava. Table 1 shows some of the starters that have been described and analyzed. The major principle of their manufacture is to prepare an uncooked dough of rice or wheat flour (sometimes mixed with cassava meal), water and a variety of herbs and spices. This dough is inoculated with a backslop and shaped into small balls or flattened tablets (cakes), which are incubated at around 30°C for about a week. During this period the niche microfloras develop and, simultaneously, the tablets dehydrate. These tablets can be stored at ambient temperatures without significant loss of viability for at least 6 months.

Studies on the microflora of starters such as Indonesian ragi (Fig. 1b) and Chinese chiu-chu have been reported as early as the end of the 19th century. The principal amylolytic moulds are Amylomyces rouxii, Rhizopus spp., Mucor spp. and Aspergillus spp. Common yeasts in many starter tablets are Hansenula spp., Saccharomycopsis fibuligera, Candida spp. and Sm. cerevisiae (Saono et al., 1996). The exact mycoflora of ragi varies with location and the particular fermentation for which the starter is to be used. A study on nearly 100 amylolytic yeast strains isolated from ragi and other starters revealed that the predominant amylolytic yeasts are Sm. fibuligera and, to a lesser extent, Saccharomycopsis malanga (Hesseltine & Kurtzman, 1990).

Selected strains of Aspergillus oryzae are used in the preparation of tane-koji in the manufacture of saké. The mould produces α-amylase and amyloglucosidase, which hydrolyze starches to dextrin, maltotriose, maltose and glucose, and acid and alkaline proteases, which hydrolyze proteins to peptides and amino acids. Other essential moulds in the production of rice wine include Aspergillus usamii and A. rouxii.

Moulds belonging to the genera Mucor and Rhizopus are usually the main enzyme producers for the production of rice wines in India and Nepal (Shrestha et al., 2002). The main yeasts which ferment saccharified rice starch to alcohol are Pichia burtonii, Sm. fibuligera, S. cerevisiae, Candida glabrata and Candida lactosa, while Sm. fibuligera produces amylolytic enzymes as well (Tsuyoshi et al., 2005). In murcha from India, Saccharomycopsis capsularis and P. burtonii also contribute to the degradation of starch (Tsuyoshi et al., 2005). Other yeast species, namely Hansenula spp., Pichia spp. and Torulopsis spp., have also been isolated from rice wine. The role of Sm. fibuligera is two-fold: it is an important amylolytic species (Dansakul et al., 2004) and it also produces alcohol, albeit at relatively low levels (Limtong et al., 2002).

In a study of yeast diversity in Thai traditional alcohol starters, 43 yeasts from 38 samples of loog-pangkao-mag (starters for alcoholic sweetened rice) and 49 from 19 samples of loog-pang-lao (starters for rice wine) were investigated (Limtong et al., 2002). Saccharomycopsis fibuligera predominated (31 isolates) in both types of loog-pang; the organism showed strong amylolytic activity but was a poor alcohol producer. Other species identified include P. anomala (8), Issatchenkia orientalis (6), P. burtonii (6), Pichia fabianii (4), Candida rhagii (4), C. glabrata (3), Torulaspora globosa (3), Pichia mexicana (2) and single isolates of Pichia heimii, Rhodotorula philyla, S. cerevisiae, Torulaspora delbrueckii and Trichosporon faecale. These have low amylolytic activity but possess high or moderately high alcoholic fermentation.

An interesting functional aspect of these fungi is their formation of functional enzymes to release assimilable carbon sources. These enzymes are valuable in brewing and flavour development. For example, glucoamylase (glucan 1,4-α-glucosidase) [EC 3.2.1.3] is a key enzyme in rice wine fermentation, converting starch directly into glucose. Glucoamylase is inducible by glucose, starch, maltose and glycerol and can degrade a variety of polysaccharides. This enables the yeast to mobilize assimilable carbon sources. On the other hand, glucosidase activity can also contribute to flavour development as a number of flavour precursors in fruits are glycosides. Esters, fusel alcohols, acids and other compounds which contribute to flavour are also produced.

Based on abilities to produce high amylolytic activities (mainly due to α-amylase and/or amyloglucosidase), a number of strains of A. rouxii, Rhizopus spp. and Saccharomycopsis spp. have been selected. For instance, a combination of A. rouxii and Sm. fibuligera produces a good quality tapé. Similarly, defined granulated starters containing A. rouxii and Sm. cerevisiae make high-quality Vietnamese rice wine (Dung et al., 2005).

Snacks and beverages

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Sweet, low alcoholic snacks

A popular type of indigenous fermented snack can be encountered in a large part of East Asia, e.g. tapé ketan, kao-mark (from glutinous rice), and tapé ketella or peujeum (from cassava roots) (see Table 1). Common features are the semi-solid consistency, the distinct sweet, mild-sour taste and the fruity flavour of alcoholic fermentation that has just started. They can be consumed as such or used as an ingredient in homecooking and baking. The principle of their manufacture involves the preparation of the substrate (glutinous rice or peeled, chopped cassava) by washing, soaking and steaming until soft; followed by cooling, inoculating with powdered starter and fermenting under cover for 1–3 days. In Indonesia, ragi tapé would be used (Ko, 1986) and in Thailand, loog-pang starter is used to prepare kao-mark (Boon-Long, 1986). The major modifications of the substrate, i.e. release of glucose from cooked starch by fungal glucoamylase, and alcoholic-organic acids fermentation and flavour formation are ascribed to a limited selection of fungi. These include A. rouxii, Rhizopus spp., Mucor spp., Sm. fibuligera, P. burtonii, P. anomala and S. cerevisiae (Boon-Long, 1986; Ko, 1986). Pichia anomala is required to develop a rich aroma and the typical flavour of tapé (Ko, 1986) by formation, for example, of isobutanol, isoamyl alcohol and their esters. The ethanol (up to 10% v/v) serves as a source of calories and helps prevent growth of disease- or toxin-producing microorganisms in the products. Although bacteria, particularly Bacillus spp. and Acetobacter spp., are present in relatively low numbers (<105 cfu g−1), they nevertheless are considered to contribute to the quality and flavour of tapé ketan (Ardhana & Fleet, 1989). In particular, the ability of Bacillus spp. to produce amylolytic and proteolytic enzymes would make a significant contribution to the degradation of macromolecular substrates, leading to its desired moist appearance and soft texture (Ardhana & Fleet, 1989).

Rice wines

Rice wines are produced from the hydrolytic breakdown products of cereal starches and other polysaccharides. They range from simple Thai rice wine to highly sophisticated Japanese saké. The moulds involved in alcohol production of Asian rice wines include A. rouxii, and the yeasts S. cerevisiae, Saccharomycopsis burtonii, Sm. fibuligera, Cm. lactosa and related yeasts. Rice and/or cereal wines are produced on both a cottage and a commercial scale in most Asian countries, especially Japan, China, Korea, Thailand, the Philippines and Vietnam (Nout & Aidoo, 2002).

Wines may be distilled to obtain a liquor or spirit, for instance the famous Indonesian brem bali, an alcoholic liquor produced in Bali from the liquid portions of tapé ketan. These liquors can also be used to fortify rice wine.

Saké is a pale yellow rice wine of Japanese origin with an alcohol content of 15–16% (weight in volume, w/v) or higher. Steamed rice is mixed with tane-koji (A. oryzae) and allowed to ferment for 5–6 days, after which it is mixed with yeast moto or ragi starter and water to form the main mash, or moromi. Moto dominates the moromi fermentation. Wild yeasts tend to die off at the early stages of moromi fermentation due to nitrite produced by nitrate-reducing bacteria.

Malaysian rice wine or tapai is lighter in colour, ranging from red to pink. It is made from cooked gelatinized rice and red pulverized ragi (yeast cake, or jui-piang).

Yakju and takju are Korean alcoholic beverages originally made from rice, but which are now made from wheat, barley, corn or millet. In the traditional yakju process, steamed, cooled rice is mixed with nuruk amylolytic starter, and yeast inoculum is added. Takju is made by diluting fresh yakju liquor prior to filtration. In comparing the traditional and industrial rice wine brewing processes in Korea, it was noted (Rhee et al., 2003) that nuruk is used in the traditional method, normally carried out at low temperatures (5–10oC). The industrial brewing follows the Japanese saké brewing method and undergoes relatively high temperature fermentation (25oC). The alcohol content in the industrial rice wine tends to be higher but the wine is lower in esters than the traditional brew.

In the Philippines, tapuy (Kozaki & Uchimura, 1990) (Igorot ethnic group) is an acidic but sweet alcoholic rice wine and is known by other names such as binubudan (Ifugao), binuburan (Ilocano) or purad (Tagalog). The Thai rice wines such as sato and krachae are cloudy yellow liquids made from glutinous rice (Vachanavinich et al., 1994).

In Vietnam, ruou nep and ruou nep than are made by steaming white or purple glutinous rice, respectively, and inoculation with men, an amylolytic starter (Table 1, Fig. 1b). Fermentation is carried out in a two-stage process of which the first stage is aerobic mould fermentation in a solid-state condition (Dung, 2004). The main alcoholic fermentation occurs during the second stage after water has been added and lasts for approximately 5 days. At the final stage, the wine is a turbid suspension of pink red colour, containing 8–14% (w/v) alcohol and some residual sugars. The wine may be clarified and/or strengthened by blending with distilled alcohol, depending on local demand.

Jnard

Jnard, or jaanr (Tamang et al., 1988), is a common name for some traditional alcoholic fermented beverages in the eastern Himalayas in India, generally produced by using murcha as a starter. Seeds of finger millet (Eleusine coracana) are boiled, drained, cooled, mixed with powdered murcha (Tamang & Sarkar, 1995) (1–2%, w/w), packed in a bamboo basket, covered and left for 2–4 days. At the end of saccharification, a sweet aroma is emitted when the mass is transferred into an earthen pot and covered to make it airtight. After fermentation, the seeds are kneaded to remove seed coats, put into a bamboo/wooden vessel and lukewarm water is added. After about 10 min, the beverage is ready to drink. Good quality jnard has a pleasant sweet aroma blended with mild alcohol (Tamang et al., 1988).

The mixed population of moulds, yeasts and lactic acid bacteria in murcha starter (Tamang et al., 1988) soon becomes active, bringing about changes in the substrate, increasing the temperature of the fermenting mass by 4°C over the ambient (20–25°C) within 2 days of fermentation. Amylase activity reaches its peak on the second day of fermentation; mucoraceous fungi have an active role in saccharification and liquefaction of starch. The moulds Mucor circinelloides and Rhizopus chinensis, and the yeast Sm. fibuligera, which are dominant at the start, disappear within 12 h of fermentation. Mature jnard contains P. anomala, S. cerevisiae and C. glabrata yeasts and lactic acid bacteria (105–106 cfu g−1), which include Pediococcus pentosaceus and Lactobacillus bifermentans. These three yeast species increase from 105 to 107 cfu g−1 within 2 days, and the population then remains the same till the end of fermentation. The titratable acidity and alcohol content of the fermenting mass increase significantly during the fermentation.

Palm wines

In almost all tropical places in Asia where palm trees grow, the sap obtained from the decapitated inflorescence of various species of palms is fermented to produce an alcoholic beverage called palm wine, or toddy. In India there are three types of toddy: ‘sendi’, obtained from wild date palm (Phoenix sylvestris); ‘tari’, from palmyra palm (Borassus flabellifer) and date palm (Phoenix dactylifera); and ‘nareli (nira)’, from coconut palm (Cocos nucifera) (Batra & Millner, 1974). The toddy from coconut flower juice is known as ‘ra’ and ‘panam culloo’ in Sri Lanka, ‘nuoudua’ in Vietnam, ‘tuak (tuack)’ in Malaysia and Indonesia, and ‘tuba’ in the Philippines.

There is an art in binding the flower spathes, pounding them to cause the sap to flow properly by cutting the spathe tip and collecting the sap into the earthen pitchers which contain yeasts and bacteria in the left-over toddy from the previous lots. The fermentation starts as soon as the sap flows into the pitcher. Palm wine is either consumed fresh as it is brought down from the tree or fermented for up to 24 h. The freshly cut sap is generally a dirty brown sweet liquid having 10–18% w/w sugar, which after fermentation results in the formation of a product containing as much as 9% (volume in volume, v/v) ethanol (Steinkraus, 1996; Joshi et al., 1999).

The palm wine fermentation is always an alcoholic–lactic–acetic acid fermentation, involving mainly yeasts and lactic acid bacteria. In the fermenting sap, S. cerevisiae is invariably present but lactic acid bacteria such as Lactobacillus plantarum, L. mesenteroides or other species of bacteria like Zymomonas mobilis and Acetobacter spp. vary. The other yeast types include Schizosaccharomyces pombe, Saccharomyces chevalieri, Saccharomyces exiguus, Candida spp. and Saccharomycodes ludwigii in the samples of coconut palm wine (toddy). Saccharomyces cerevisiae, Sch. pombe, Kodamaea ohmeri and Hanseniaspora occidentalis are characterized as maximum ethanol producers in toddy (Joshi et al., 1999). The yeasts, especially Saccharomyces spp., are largely responsible for the characteristic aroma of palm wine (Uzochukwu et al., 1999). During fermentation, there is continuous effervescence as a result of the production of carbon dioxide. A yeasty odour develops, and after a couple of hours yeasts form a sediment at the bottom of the container. The main ingredient of the fresh sap (pH ∼7.2) is sucrose (12–15%, w/w). During the first 24 h, more than half of the total sugars are fermented. Palm wine is a good source of B vitamins.

Kombucha

Kombucha from Central and East Asia is a beverage obtained by fermentation of sweetened boiled tea with a mixed culture of yeasts and acetic acid bacteria (Campbell-Platt, 1987). Other names for kombucha, or ‘tea fungus’, include ‘fungus japonicus’, ‘tee kwass’, ‘tea kvass’, ‘champignon de longue vie’, ‘Indo-Japanese tea fungus’ and ‘Manchurian mushroom’. Kombucha is a symbiosis of Acetobacter spp. – mainly Acetobacter xylinum– and various yeasts. The mixed yeast-bacterial culture growing on sugary tea extract accumulates lactic (0.1%), acetic (traces) and gluconic (0.01–0.3%) acids, and some ethanol (0.3%). The pH decreases steadily to about 2.5. The resulting beverage also contains vitamins and minerals and is considered to be a healthy product.

The yeast flora of commercial tea fungus includes the genera Brettanomyces (56%), Zygosaccharomyces (29%) and Saccharomyces (26%) (Mayser et al., 1995). Saccharomycodes ludwigii and Candida kefyr (anamorph of Kluyveromyces marxianus) in isolated cases, as well as a pellicle-forming yeast, C. krusei and apiculate yeasts, Kloeckera spp. and Hanseniaspora spp. have also been reported. However, Zygosaccharomyces kombuchaensis is the dominant yeast species now known to be commonly associated with kombucha tea (Kurtzman et al., 2001). In another study of four commercial kombucha products (Teoh et al., 2004), the yeasts found included Brettanomyces bruxellensis (anamorph of Dekkera bruxellensis), Candida stellata, Sch. pombe, T. delbrueckii and Zygosaccharomyces bailii. Comparing these findings, it appears that the fermentation is initiated by osmotolerant yeasts and is then succeeded and ultimately dominated by acid-tolerant species.

Condiments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Wadis

Wadis, traditionally consumed in Punjab and Bengal of India, are now popular in many places of India, Pakistan and Bangladesh. These dried, hollow, brittle cones or balls (3–8 cm diameter, 15–40 g in weight) (Fig. 1c) are used as a spicy condiment or an adjunct for cooking vegetables, grain legumes or rice.

To prepare wadi, dals, generally of blackgram, are soaked, drained, ground into a smooth soft dough, left to ferment for 1–3 days, moulded into cones or balls, deposited on bamboo or palm mats smeared with oil, and sun-dried for 4–8 h. The surface of the cones or balls becomes covered with a mucilaginous coating which helps to retain the gas formed during their fermentation. The wadis look hollow, with many air pockets and yeast spherules in the interior and a characteristic surface crust.

Initially the microflora is diverse and contains lactic acid bacteria, bacilli, flavobacteria and yeasts. Gradually, L. mesenteroides, L. fermentum, S. cerevisiae and Tr. cutaneum become dominant. Candida vartiovaarae and K. marxianus are also often found. The development and prevalence of microflora are affected by the seasons, summer being more favourable for bacteria and winter for yeasts. The production of acid and gas results in a fall of pH from 5.6 to 3.2 and two-fold rise in the volume of the dough. The lactic acid bacteria are mainly responsible for the acidification of dough, favourable conditions for the yeasts to grow and become active for leavening. The fermentation brings about a significant increase in soluble solids, non-protein nitrogen, soluble nitrogen, free amino acids, proteolytic activity and B vitamins including thiamine, riboflavin and cyanocobalamine. On the other hand, the levels of reducing sugars and soluble protein decrease. Amylase activity increases initially, but declines thereafter (Batra & Millner, 1974; Sandhu et al., 1986; Sandhu & Soni, 1989). Wadis prepared by inoculating sterilized ingredients with a mixed culture of C. krusei (anamorph of Issatchenkia orientalis) and L. mesenteroides resemble the marketed ones. In contrast, the uninoculated controls were hard and compact and, when broken, had a glistening surface (Batra & Millner, 1974).

Papads

Papad (papadam) is another important condiment or savoury food in India, Pakistan and Bangladesh. This thin, usually circular, wafer-like product (Fig. 1d) is used to prepare curry or is eaten by itself as a crackly snack or appetizer with meals after roasting or deep-frying in oil. Papad-making under controlled conditions has already developed into a cottage or small-scale industry.

Blackgram flour or a blend of blackgram with Bengalgram, lentil (Lens culinaris), redgram or greengram (Vigna radiata) flour is hand-kneaded with a small quantity of peanut oil, common salt (about 8%, w/w), ‘papad khar’ (saltworts produced by burning a variety of plant species, or from very alkaline deposits in the soil) and water, and then pounded into a stiff paste. The dough (sometimes with a backslop and spices added) is left to ferment for 1-6 h. The fermented dough is shaped into small balls which are rolled into thin, circular flat sheets (10–24 cm diameter, 0.2–1.2 mm thick) and generally dried in the shade to 12–17% (w/w) moisture content. Candida krusei and S. cerevisiae are involved in the preparation of papad (Shurpalekar, 1986).

Soy sauces

Soy sauces are light to dark brown liquids with a meat-like salty flavour used in cooking and as a table condiment. Traditionally made in China, Japan, Korea, Thailand, the Philippines, Indonesia and Malaysia, soy sauce is now also produced in Europe and the Americas. There are two specific fermentation stages involved in soy sauce production: aerobic koji fermentation, which involves the use of A. oryzae or Aspergillus sojae, and an anaerobic moromi or salt mash, which undergoes lactic acid bacteria and yeast (Zygosaccharomyces rouxii) fermentations.

The two main groups of enzymes produced by A. oryzae during koji fermentation are carbohydrases (α-amylases, amyloglucosidase, maltase, sucrase, pectinase, β-galactosidase, cellulase, hemicellulase and pentosan-degrading enzymes) and proteinases. Lipase activity has also been reported. These major enzymes hydrolyze carbohydrates and proteins to sugars and amino acids and low molecular weight peptides, respectively. These soluble products are essential for yeast and bacterial activities during moromi fermentation (Aidoo et al., 1994; Chou & Rwan, 1995). In this fermentation Tetragenococcus halophila initially proliferates and produces lactic acid, which lowers the pH to 5.5 or less. Acid-tolerant dominant yeasts, notably Z. rouxii, grow and produce about 3% (w/v) alcohol and several compounds which add characteristic aroma to soy sauce.

Although Z. rouxii is the dominant moromi yeast which produces alcohol and several compounds that add characteristic aromas to soy sauce, other yeasts such as Candida versatilis and Candida etchellsii also produce phenolic compounds, i.e. 4-ethylguaiacol and 4-ethylphenol, which contribute to soy sauce aroma. Nearly 300 types of flavour compounds have been identified in Japanese soy sauce (Nunomura & Sasaki, 1992). Zygosaccharomyces rouxii produces flavour compounds including alcohols, glycerol, esters, 4-hydroxy-5-methyl-3(3 H)-furanone (HMMF), 4-hydroxy-2 (or 5)-ethyl-5(or 2) -methyl-3(2 H)-furanone (HEMF) and 4-hydroxy-2,5-dimethyl-3(2 H)-furanone (HDMF). Of the furanones, HEMF produced by Z. rouxii and Candida spp. gives Japanese-type soy sauce its characteristic flavour (Hanya & Nakadai, 2003). This compound is also reported to have antitumour and antioxidative properties (Nagahara et al., 1992; Koga et al., 1998). Higher alcohols such as isobutyl alcohol, isoamyl alcohol and 2-phenyl ethanol, produced by C. versatilis, are also important flavour constituents of soy sauce. Certain strains of yeasts have deleterious effects on soy sauce. Film-forming yeasts, mainly belonging to the genera Zygosaccharomyces, Hansenula and Pichia, cause spoilage in moromi fermentation.

Miso

Miso is a salty paste with a meat-like flavour made by fermenting soybean, with or without the addition of rice or barley, using A. oryzae and a yeast, Z. rouxii. Sometimes, Tetragenococcus halophila and Enterococcus faecalis are also involved in the fermentation. Miso is a seasoning agent and is also used in the preparation of miso soup. Heat-treated rice and/or soybeans are used to prepare ‘shinshu’ or rice-soybean miso. After the initial solid-substrate fermentation dominated by A. oryzae, salt (38% of the original weight of dry soybeans) is added to the koji and mixed thoroughly. The mixture is backslopped or inoculated with Z. rouxii and allowed to ferment for up to 15 days for sweet miso and 2–12 months for salty miso. Although other halophilic yeasts such as Torulopsis versatilis may be present, only Z. rouxii produces the desired metabolites for an acceptable product (Ebine, 1989). Flavour components in miso are similar to those of soy sauce. Furanones, HEMF and HDMF, produced by Z. rouxii, have been identified as important flavour components in miso. Miso also contains B vitamins (riboflavin and cyanocobalamine) as a result of yeast fermentation.

Future perspectives

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References

Upgrading of traditional home-scale processes is needed so that they can continue to maintain and strengthen the cultural heritage and can compete successfully with imported products. Whereas small-scale manufacture has the advantages of short distribution lines, income generation for families, etc., urbanization and the resulting growing demand for ready-to-consume high-quality foods requires larger-scale controlled industrial production. Examples of industrialized traditional fermented foods (Steinkraus, 1989) are:

  • i
    alcoholic snacks such as tapai, which are now produced at a small cottage scale in Malaysia using commercially available pure culture starters of the starch-degrading mould A. rouxii and the yeast Sm. fibuligera;
  • ii
    rice wines such as Japanese saké, using A. oryzae for rice saccharification and saké yeasts (S. cerevisiae strains selected for reduced foam production, or killer properties if required);
  • iii
    condiments such as soy sauce inoculated with Z. rouxii and Candida spp. and miso in which similar halotolerant yeasts are used for flavour development.

Yeast products such as enzymes, B vitamins, trace elements (selenium, chromium), glycans, flavour components and carotenoid pigments occur in traditional foods, but could be exploited more effectively as purified substances and food ingredients. Yeasts have a relatively high content of protein, lipids and micronutrients. In view of the widespread micronutrient deficiencies in regions that depend predominantly on plant-based diets, the addition of yeast-derived food products could contribute to improved nutritional status (Mai et al., 2002).

In conclusion, a wide variety of yeasts are involved in traditional fermented foods. Although the occurrence of various yeasts has been reported, knowledge and understanding of their ecology including aspects such as microbial successions and competitiveness, and of their genetic and physiological properties remain to be acquired. In particular, yeasts that contribute to desirable product properties require more precise characterization, using genomics, proteomics and physiological approaches for more efficient identification and exploitation, while developing consumer-friendly strategies to control fermentations and safeguard hygiene.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Pancakes and breads
  5. Amylolytic fermentation starters
  6. Snacks and beverages
  7. Condiments
  8. Future perspectives
  9. References
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