1

Origin and History of Food Fermentations

Keith H. Steinkraus
Cornell University, Ithaca, New York, U.S.A.

If you know the history of mans food, you know the history of man. KHS

I.

INTRODUCTION

According to current scientic thought, the universe is approximately 15 billion years old and the Earth is approximately 4.5 billion years old. Fossil microorganisms have been found in rocks 3.3 to 3.5 billion years old (1). They were the rst forms of life to appear on Earth. They were likely the blue-green algae, which contain a pigment enabling them to use the suns radiation to synthesize carbohydrates. They contain deoxyribonucleic acid (DNA) and ribonucleic acid (RNA) similar to all other forms of life today. They also contain the enzymes, proteases, amylases, lipases, and other enzymes required to hydrolyze proteins, starches, and lipids necessary for recycling. This was very fortunate because microorganisms have been required ever since as recyclers of organic matter. Without them, the Earth would be a giant dumping ground containing all forms of organic matter and dead bodies. Initially, microorganisms consumed organic matter, including dead organisms, as food for their own energy requirements. Later, after plants and animals evolved, microorganisms consumed dead plants and animals and became able to invade plants and animals, causing diseasein some ways the rst stage in recycling. The next forms of life, evolving about a billion years later, were plants, also based upon DNA/RNA and having the ability to convert carbon dioxide and water to carbohydrates using the suns radiation for energy. The plants became the food supply for future evolution of animals, including humans. Microorganisms recycled the plants, consuming them as food/energy as they died, returning them to soil for future plant growth. Plant life evolved in a sea of microorganisms and thus had to have means of resisting invasion (plant disease) even when alive. They did this by developing a ligno-cellulose structure that resists microbial invasion. A seed germinating in the soil has to survive the onslaught of billions of microorganisms that, given the opportunity, would destroy the seed and/or recycle the developing plant. Plants, their leaves and rootscassava, sweet potatoes, yamsberries,

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fruits, nuts and cereal grainsparticularly wheat, rice, maize, barley, rye, oats, millet, and sorghumand legumes, beans, and peas are major staples of our food supply today. Millions of years before humans appeared on earth, all the chemical and enzyme reactions needed for food fermentations were present as part of the recycling reactions used by microorganisms to digest and recycle plant components; for example, fermentation of fruits and fruit juices to wine and vinegar, germination of grains as the rst step in brewing alcoholic beverages, and souring of milk. When humans and other animals evolved on Earth, they had to consume the food supply either before it was invaded by microorganisms and recycled or while in various stages of recyclingthe fermented foods. When microbes produced unpleasant aromas or avors in the food or produced toxins that caused illness or death, the food was spoiled and humans learned to avoid it. If the invasion of the food components by microorganisms yielded attractive aromas, avors, and textures, humans learned to appreciate and desire such foods. These were the beginning of fermented foods, including sour milk, cheeses, wines and beers, vinegar, lactic acid products such as sauerkraut, and hundreds of other fermented foods consumed today. There is another factor related to fermented foods and lost in antiquity, and that is salt: common salt, sodium chloride, or sea salta mixture of sodium, potassium, magnesium, and calcium salts found in seawater. Salt has been highly prized for thousands of years. In ancient times, soldiers received part of their pay in the form of salt (or salary) and, even today salt is vital to producing savory foods, based primarily on its condiment value, but it was also valued throughout history as a preservative. Salt in suitable concentrations, prevents putrefaction and leads to a controlled protein hydrolysis. When ponds of seawater dry up under the inuence of temperature and wind-ow (actually a method of producing sea salt even today), the seawater may contain sh and other sea animals that isolated in the seawater die their bodies are self-autolyzed by their enzymes, leading to amino acid/peptide concentrations. It is likely that humans discovered that such animal residues in high salt brines were savory condiments. Humans also discovered very early that salt could preserve sh or other animal tissues, especially when they were sun-dried, and such salted, sun-dried sh are staple foods in many marine areas of the world today. Seawater also may have played a role in primitive lactic acid fermentation/preservation of plant materials because such materials stored in seawater would likely undergo lactic acid fermentation as well. It has been hypothesized by anthropologists (2) that it was alcoholic fermentation and the desire for alcohol that motivated humans to settle down and become agriculturists. Humans could not have survived over the millennia without fermented foods. Fermentations preserve foods, improve digestibility and enrich substrates with essential vitamins, amino acids, and fatty acids. They also convert vegetable proteins to savory meat-like avors and textures and yield the diverse avors and aromas that enriched the human diet in the past, enrich our diets today, and will continue to do so in the future.

II. HISTORY OF SELECTED FERMENTED FOODS A. Alcoholic Fermentations

Mead/Honeywine. Honeybees have been producing honey from owering plants and probably also from honeydew for 10 to 20 million years before humans appeared on earth (3). Honey was the worlds rst concentrated sweet. Its sugar concentration (about 80%) is too high for honey to undergo fermentation or even spoilage without dilution. It was the reserve food for the honeybees themselves but also sought after by humans and animals such
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History of Food Fermentations

as bears. Diluted with water such as rain, however, it will undergo fermentation by yeasts that live in the surrounding environment. So it is likely that honey/mead fermentation was occurring long before humans arrived and continues as a fermentation today. Primitive wines and beers are vastly dierent from our modern wines and beers. The former are generally cloudy, eervescent beverages containing not only liquid but particles of the fermenting substrate, yeast cells along with the alcohol, and B vitamins. They are very nutritious and energy-rich. An example is African kar/sorghum beer. The art of kar beer production goes back to prehistoric times. In the villages, kar beer is made by women: girls learn how to make kar beer for their husbands before they marry (4). Sorghum grains or millet are germinated, sundried, ground, and mixed with sorghum, millet, or maize ours and water, and then cooked, cooled, and fermented by the residual yeasts and the dregs in the containers. Fermentation is carried out in large crocks or drums (5). Fermentations involving production of ethanol are among the most ancient fermentations known. The most primitive methodology utilizes chewing the grains to introduce saliva (ptyalin) as a source of amylase to hydrolyze the starch to sugar and has been used for centuries. An example is chicha, produced in the Andes region of South America (6). Even today, women and children sit in a circle chewing maize kernels. The gobs are then removed from the mouth and sundried. Later they are placed in crocks covered with water and allowed to ferment with yeasts in the environment. The yellow colored cloudy liquid contains as much as 6% ethanol and a wide variety of B vitamins. In ancient Incan times, the emperor himself could hold oce only as long as he delivered sucient chicha to the citizens. In ancient Japan, rice wine/sake was also produced using chewing of grains as a source of amylase to convert the starch to sugar (7). Later it was discovered that rice overgrown with Aspergillus, Rhizopus, or Mucor molds also became sweet and could be fermented to rice wine. Among the more complex sweet/sour alcoholic foods are tapay, tapai, tape and Chinese Lao-chao. These generally rely on two or more fungi for their production. These can include Amylomyces rouxii, a yeast-like mold, and Endomycopsis buliger, a mold-like yeast (8). Thousands of years ago in Egypt, wheat grains/our were made into lightly baked bread that was then moistened with water and fermented to a primitive beerbouza. Still earlier in human history, at the dawn of agriculture, when grains were collected in crocks, it is highly likely that such grains, on occasion, became moistened with rain, germinated, and fermented to primitive beers. The most ancient Mexican alcoholic beverage is pulque, made by fermenting pulp juices from the Agave plant. Leuconostoc mesenteroides produces dextrans that add texture to the beverage. The alcohol is produced by Saccharomyces cerevisiae, a yeast, or by Zymomonas mobilis, an alcohol-producing bacterium. Pulque is very rich in B vitamins and plays a vital role in the nutrition of, in particular, the economically disadvantaged in Mexico (4). B. Vinegarthe Acetic Acid Fermentation

Primitive alcoholic beverages generally contain some acetic acid, but the amount is limited as long as the fermentation remains anaerobic. The rapid production of carbon dioxide helps maintain anaerobiosis by providing a layer of CO2 on the surface of the fermenting materials. However, when the alcoholic fermentation stops, Acetobacter sp. become active as soon as oxygen becomes available, and a portion of the ethanol is converted to acetic acidvinegar. Vinegar is an ancient condiment and extremely useful as a pickling agent or even as a medicinal because it is germicidal.
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Savory/Meat Flavored Sauces and Pastes. It is not known who discovered how to transform bland vegetable protein into meat-avored sauces and pastes. It may have been an accident; nevertheless, it was one of the great discoveries in food science. When seeds fall upon the ground, they either germinate, forming new plants, or they become overgrown with microorganisms as the rst step in recycling. The seed coat is rather resistant to microbial growth, so the rst organisms to penetrate into the cotyledons are often molds that produce proteases, lipases, and amylases that hydrolyze the various components in the seed. Thus, the moldovergrown seeds become a source of enzymes. Of scientic importance, such moldy seeds are described as a koji and can be used to hydrolyze the proteins, lipids, and starches in other vegetable or animal products. The rst koji in recorded literature was a millet kogi. Millet koji was mixed with meat, sh, or fowl and salt and stored in a bottle for 100 days. The rst reference to meat-avored pastes was made about 3000 years ago during the Chou dynasty in China (9). The rst reference to soybeans as a substitute for meat was in the worlds oldest encyclopedia of agriculture, published in A.D. 535 in China. Soybeans, rich in protein, are an excellent source of nutrition. In order to be palatable, they must be hydrated/soaked and cooked. As long as soybeans remain dry they are not susceptible to microbial spoilage. After being hydrated, however, they become susceptible to overgrowth by bacteria and molds, as is true of most seeds. The rst savory products were all mashes or pastes. It was not until about A.D. 25220. that liquid sauces appeared in the literature in the Han dynasty (9). In a simple primitive process of producing savory soybean paste, soybeans are soaked and cooked and made into a ball covered with rice straw and placed under the ceiling of the house where it is warm. Aspergillus molds present in the straw overgrow the soybeans in approximately 30 days. The mold-covered soybeans are then mixed with sea salt brine and allowed to digest for a year or longer. Enzymes from the mold digest the proteins, lipids, and carbohydrates, yielding savory amino acid/peptideavored soybean paste. Liquid released from the soybean paste is a tamari-type soy sauce very rich in savory amino acid/peptide avors (10). We can only guess what eect soybean paste and soy sauce had on consumers used to eating predominately bland rice. It was one of the great discoveries of food science, and ` Maggi-type meat avors and bouillon along with soy sauce and miso we have Nestle cubes in todays markets. C. Fermentations Yielding Meat-like Textures

Indonesian tempeh fermentation is closely related to soy sauce fermentation as the rst stage is an overgrowth of soybeans with a mold, Rhizopus oligosporous or related strains (4,11,12). The fungal mycelium knits the soybean cotyledons into a compact cake that can be sliced thin and deep-fat fried or cut into cubes for use in soups. This fermentation has been carried out in Indonesia for hundreds of years by people untrained in microbiology or chemistry yet they have the ability to produce high-quality tempeh. The most surprising thing about tempeh fermentation is that in recent years a new high-technology industry has developed with the objective of producing meat substitutes (4,1315). There are two major methods. The rst is to extract soybean protein and spin it into bers by passing the protein strands through a chemical bath. The resulting bers are oriented to a meat-like texture and meat avors are added. The dehydrated chunks are used in soups and other food products as vegetarian meat substitutes. It is a very sophisticated and relatively expensive food processing technique. Indonesian tempeh achieves much the same objective by fermentation in which mold mycelium provides the

Copyright 2004 by Marcel Dekker, Inc. All Rights Reserved.

History of Food Fermentations

meat-like texture and the resulting products are within the nancial means of the average Indonesian. A second method of producing meat substitutes is even more closely related to the tempeh process in that it involves growing edible strains of Fusarium graminearum mold mycelium, harvesting the mycelium by centrifugation/ltration and adding meat avors, and then dehydration. This process was developed by Rank, Hovis, MacDoughall (RHM) in England (16,17). The nuggets are based on mold mycelium for texture plus added avors. This technology is advanced and sophisticated and relatively expensive compared to the tempeh process. Indonesian tempeh achieves a similar degree of texture as a meat substitute by overgrowing soaked, dehulled, cooked soybean cotyledons with Rhizopus oligosporous mycelium. D. Lactic Acid Fermentations

Lactic acid fermentations are among the most ancient and important fermentations in the world: they enabled the human race to survive and thrive and they remain very important in the diets of humans today (4). Lactic acid fermentations became known to humans as soon as they started domesticating and milking cows, sheep, and goats. People had to store the milk in a container, and one of the earliest containers was the stomachs of slaughtered animals. Milk sours very rapidly because of its natural content of lactic acid bacteria. Sour milk became one of the rst fermented foods after humans settled down and became agriculturists, and it lives on in the form of yogurts today. Stored in animal stomachs, the sour milk curdled, lost its whey, and became primitive cheeses through the activities of other lactic microorganisms in the environment. For millennia, cheeses have been an important part of the diet of humans and they remain so today. Lactic acid fermentations are very energy ecient, generally requiring no heating or cooking either before or after fermentation. A prime example of lactic acid vegetable fermentations is the sauerkraut fermentation. Fresh cabbage is shredded and mixed with 2.25% w/w salt (sodium chloride). The salted cabbage is placed in a crock and covered with a lid or a plastic cover that allows no penetration of air. The natural fermentation (no inoculum required) begins with the development of Leuconostoc mesenteroides. L. mesenteroides produces both lactic acid and carbon dioxide, which ushes out any residual oxygen, helping to maintain anaerobic conditions. The second organism that develops is Lactobacillus brevis, which produces additional lactic acid and carbon dioxide. This is followed by Lactobacillus plantarum, which produces additional acid. The last organism to develop is Pediococcus cerevisiae, which produces additional acid. The nal product has an acidity of about 1.7% to 2.3% acid (as lactic) and has excellent keeping quality as long as the product is kept anaerobic. The sauerkraut can be eaten fresh without cooking as a salad or cooked as a hot food. Another lactic acid fermentation is that of Korean kimchi, which is a staple in the diet of the average Korean, who may eat 100 g a day in summer and 150 g a day in the winter. In Korean kimchi, Chinese cabbage is a prime substrate but radishes, red peppers, and other vegetables may be included. The vegetables are shredded and immersed in a strong salt brine (57% salt for 12 hours or 15% salt for 37 hours) followed by draining and rinsing. The subsequent fermentation time depends on the temperature of fermentation (one day at 30jC or 360 days at 5jC). Kimchi is less acidic than sauerkraut and the product is carbonated.

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Lactic acid fermentation has been applied to most vegetables such as cucumbers and carrots, and some green fruits, such as limes and olives. It has been utilized by Indian farmers to preserve excess vegetables during the growing season. Lactic acid fermentation is utilized throughout the world as a prime method of preserving fresh vegetables. It is likely that bread fermentations began as soon as humans started to use re/ cooking and grinding starchy grains such as barley, wheat, millet, rye, and sorghum to make them more easily consumed. Such ours slurried with water, immediately begin to ferment by lactic acid organisms and yeasts in the environment. These microorganisms struggle for survival in the increasingly acidic mixture. The outcome generally includes one or more lactic acid species and one or more yeasts. If the our-water slurry is dense enough to form a dough or pancake-like structure and it is baked, it will yield, depending on the conditions, leavened or sourdough-like breads. Since at least 5000 B.C., breads have played a signicant role in human diets. Wheat ours contain gluten, which retains the carbon dioxide produced by heterofermentative lactic acid bacteria and yeasts fermenting symbiotically. Rice does not contain gluten, so it cannot yield leavened bread, but people from the region known today as India discovered a way of producing bread-like foods from rice by combining fermentation of rice with that of legumes such as black gram. Both ingredients are soaked in water and then ground in a mortar to make a sti batter that when incubated overnight is leavened (rises) so that it can be steamed (Indian idli) or cooked as a pancake (Indian dosa) adding leavened breadlike products to the Indian diet (4).

III.

SUMMARY

Fermented foods go back to the origins of microorganisms, the rst forms of life on Earth followed by the evolution of plantsthe basis of human foodsand the subsequent interrelationships between microorganisms that have the task of recycling organic matter and the plants upon which humans and all animals depend for food and energy. Plants and plant materials (foods) are subject to recycling by microorganisms as soon as grown. If they are harvested and consumed immediately (e.g., fresh fruits and berries), there has been little, if any, fermentation or recycling. Recycling and fermentation are acceptable as long as the products are attractive in avor and aroma and do not contain any toxic products. If the avors and aromas are unacceptable to the consumer or the plant materials contain toxic material, the potential foods are described as spoiled. Fermented foods are consumed in various stages of recycling. The human race has been dependent on acceptable degrees of recycling and food fermentation from the beginning of history and remains dependent still today, although modern technologycanning, freezing, and dehydrationenables humans to postpone recycling and preserve foods for extended periods of time. The human race has depended upon fermented foods as major sources of food and energy over millennia, continues to do so today, and will do so for the future.

REFERENCES
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History of Food Fermentations

4. KH Steinkraus. Handbook of Indigenous Fermented Foods. 2nd edition. Marcel Dekker, New York. 1996. p. 776. 5. BS Platt. Some traditional alcoholic beverages and their importance in indigenous African communities. Proc. Nutr. Soc. 14:115124. 1955. 6. A Escobar. The South American maize beverage chicha. Masters Degree Thesis. Cornell University, Ithaca, New York. 1977. 7. K Yoshizawa and T Ishikawa. Industrialization of sake fermentation. In: Industrialization of Indigenous Fermented Foods. Editor: KH Steinkraus. Marcel Dekker Inc., New York, 1979. pp.127168. 8. KH Steinkraus. Nutritionally signicant indigenous fermented foods involving an alcoholic fermentation. In: Fermented Foods and Beverages in Nutrition. A Nutrition Foundation Monograph. Editor: WJ Darby and CF Gastineau. Academic Press. 1979. pp. 3659. 9. D Fukashima. Industrialization of fermented soy sauce production centering around Japanese shoyu. In: Industrialization of Indigenous Fermented Foods. Editor: KH Steinkraus. Marcel Dekker Inc., New York. 1989. pp. 188. 10. W Shurtle and A Aoyagi. The Book of Miso. Autumn Press. Kanagawa-ken, Japan. 1980. p. 254. 11. W Shurtle and A Aoyagi. The Book of Tempeh. Harper and Row, Publishers, New York. 1979. p. 173. 12. W Shurtle and A Aoyagi. History of Tempeh. The Soyfoods Center, Lafayette, California. 1984. p. 81. 13. AD Odell. 1966. Meat analoguesa new food concept. Cornell Hotel and Restaurant Administration Quarterly. 7:2024, 1966. 14. FE Horan. Meat analogues. In: New Protein Foods. AM Altschul, ed. Vol. 1A. Academic Press, New York. 1974. pp. 366413. 15. OB Smith. Extrusion-Cooked Foods. In: Encyclopedia of Food Science. (MS Peterson, and AH Johnson, editors). Avi Publishing Co., Westport, Connecticut, 1978. pp. 245250. 16. G Edwards. Myco-proteinthe development of a new food. Food Lab. Newsletter. May 21 24. 1986. 17. G Campbell-Platt and PE Cook. Fungi in the production of foods and feed ingredients. J. Appl. Bact. Symp. Suppl. 111:7S131S. 1989.

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