Roles in food

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Unlike plants and animals, the direct consumption of eukaryotic protists is often only a minor part of human diet. Protists that we eat are mainly the carpophores of Dikarya macromycetes (see page 195 and figure 360) and Rhodophyta (see page 272) or Phaeophyta (see page 331). However, some additional yeast-based products such as Marmite or Vegemite (Figure 361) are also consumed.

On the other hand, eukaryotic microbes are widely used in the manufacture of food, including that traditionally produced for a very long time. Eumycota fungi are the main protists to have been used, and in our Western societies, Saccharomyces cerevisiae (Box 16), a Saccharomycotina of the Ascomycota phylum, holds pride of place in the fungal-based food industry because it is used in the manufacture of bread and in that of alcohols: beers, wines, ciders… It has been cultivated by man for more than 9,000 years to make wine in Asia Minor, more than 6,000 years to ferment beer in Babylon and over 2,000 years to bake bread in Egypt.

The manufacture of alcohols are complex processes which often involve several microorganisms, successively or in concert. For example, Japanese sake is made using Aspergillus oryzae, belonging to the Eurotiomycetes of the Ascomycota, to hydrolyze rice starch into glucose; this will then be fermented into alcohol by yeasts. Saccharomyces cerevisiae remains the most used species because of its ability to make the two most consumed drinks: wine and beer. Yeasts that have different names like Saccharomyces ellipsoideus or Saccharomyces carlsbergensis, used respectively to make wine and beer, are just different strains of Saccharomyces cerevisiae. However, in hot countries, Schizosaccharomyces pombe a Taphrinomycotina species with a higher optimum growth temperature, is used. It is used for example to make beer in Africa. It is the alcoholic fermentation metabolism of Saccharomyces cerevisiae that allows the production of alcohol, even in the presence of oxygen. Indeed, most organisms prefer to breathe rather than ferment when given the choice between the two metabolism pathways. Saccharomyces cerevisiae uses fermentation probably in order to eliminate its competitors. Indeed, it is very resistant to alcohol because it supports up to 12-14% of alcohol by volume while most species die if the level is above 1-2%. Its production therefore makes it possible to control the growth of other microorganisms present in the fermentation medium. When the medium is depleted of sugar, Saccharomyces cerevisiae makes a dialsic transition and uses alcohol as a source of carbon in respiration.

Historically, wine appears to be the first manufactured alcoholic drink. For its production, bunches of red or white grapes are used. After harvest, they are crushed to break the skin and collect the juice. For red wine, fermentation takes place in the presence of the skin and pips, while for white wine, only the juice is fermented, because the skin and pips contain a large amount of tannins which confer color. Fermentation takes place in open barrels or controlled fermenters. Formerly, no yeast was added, a strong argument that supports the theory that making wine is the first use of yeast because the process does not require the addition of exogenous yeast, unlike making bread and beer. Saccharomyces cerevisiae is present in small quantities on grapes but a few days after fermentation, it often becomes the predominant species. Nowadays, specific strains are inoculated to have reproducible quality. The high sugar content of the juice causes the yeast to grow rapidly and results in anaerobic growth. This combined with the acidity of the grape juice and the build-up of ethanol prevents the proliferation of other microorganisms. The addition of sulphites by the winegrower further inhibits the growth of other microorganisms. After fermentation, which lasts a few weeks, an alcohol level of 10-14% is reached. The growth of the yeast is then inhibited. The amount of remaining sugar gives the more or less pronounced sweet taste of the different wines. Alcohol (ethanol) and carbon dioxide are the main byproducts but several hundred other products are synthesized, including esters, other alcohols than ethanol, organic acids… These give different tastes to wine. After the fermentation phase, the wine is transferred to barrels for aging. Bacteria then ensure additional slow fermentation. This takes at least a year. The wine is then filtered to make it sterile and bottled.

For beer, the starting material is mainly starch from barley. This must first be hydrolyzed to sucrose so that it can then be fermented. The barley grains are therefore immersed in water to allow their germination. During germination, the enzymes in the grain begin to hydrolyze the starch. The grains are then killed and dried, but the enzymes are not destroyed. This dry product is called malt. Malt can be stored for a long time and therefore beer production is less seasonal than wine. For the manufacture of beer, the malt is ground and put in hot water to give a paste called mash. Placed at 65°C for a while, the enzymes continue the hydrolysis of the starch. After incubation, the liquid, rich in sugar, is recovered. Hops, the dried flowers of Humulus lupulus, are added to impart bitterness. The liquid is boiled and the residues which have precipitated, such as proteins, are removed. Fermentation can then occur by adding yeast and is done in large vats. Different strains of yeast are used to produce different beer types, such as ale or lager.

The same protocol as the fermentation of wine is applied for making cider from apples or pears. For strong alcohols, fermentation is followed by distillation in order to concentrate the alcohol. This is the case for rum from the fermentation of sugar cane, whiskey from malt fermentation (Figure 362) or even potato, rye or sugar beet vodka. Table 14 summarizes the consumption of alcoholic beverages reported in liters of pure alcohol in some countries in 2001. The sums involved are colossal and the monetary and societal cost in terms of public health too. In France, the social cost of alcohol is estimated at 17 billion euros, or about 300 euros per person per year, of which 10 billion correspond to treatment for alcoholism and the resulting illnesses. Note, however, that in France we consume about half the alcohol per capita than 50 years ago!

For the production of bread, the most widely used flour is that of wheat, resulting from the grinding of grains and the removal of unwanted particles. It is mixed with water, and salt to inhibit the growth of yeasts. The dough is kneaded well to homogenize and to soften the gluten, a wheat protein. Everything is incubated for a few hours and then cooked. The carbon dioxide generated ensures the vacuolized appearance of the crumb by its expansion and the ethanol is eliminated by evaporation. Yeast ensures the production of other compounds that impart flavor and hydrolyze others, giving the bread its final texture. Bread has long been the staple food in Western countries. It continues to be a daily expense for many Europeans. In France alone, 10 billion baguettes are consumed per year! A French person consumes an average of 160 grams of bread per day for an annual global market of 56 billion euros…

Cheese is another food that requires Eumycota fungi for its manufacture. Initially used to preserve milk, their manufacture has become an art protected by controlled appellations. The first step in curdling the milk does not involve fungi. On the other hand, their refining involves a procession of microorganisms including yeasts and various filamentous species mainly Ascomycota such as Penicillium roqueforti, Penicillium camemberti, Geotrichum candidum, Debaryomyces spp., Fusarium spp., Scopulariposis spp., but also Mucoromycotina such as Mucor fuscus or Mucor lanceolatus. The fungi, through their lipolytic and proteolytic activities, will give each cheese its appearance, texture, taste and odor. In general, a main filamentous fungus has the primary role, for example for blue cheese made with Penicillium roqueforti (Figure 363). In France, nearly 40% of the produced milk is processed into some 1,200 different cheeses. Cheeses represent around 5% of French food expenditure for a total of close to 3 billion euros per year…

Several other important foods in our Western societies require fungi for their formation. For example, to make chocolate, cocoa beans must be fermented with a cocktail of yeast and then bacteria. Yeasts, including the Saccharomycotina Hanseniaspora guilliermondii, Hanseniaspora opuntiae, Saccharomyces cerevisiae, Kluyveromyces marxianus, Pichia membranifaciens, Pichia kudriavzevii and various Candida spp., will undergo alcoholic fermentation which will kill the seed and start its degradation. The action of these fungi will allow the development of lactic and acetic bacteria which, in collaboration with other yeasts or even filamentous fungi, will produce the complex aromas found in chocolate. Currently, the world chocolate market weighs 95 billion euros annually! Sausages are another food that require the action of fungi, such as Penicillium nalgiovense or Penicillium salamii. Other fermented meat products also use fungi for their production.

Eastern societies also use fungi a lot to make food from fermented plants. For example, the Japanese miso that is used to make soups of the same name is produced by fermenting soybeans. The beans are inoculated with various Aspergilli such as Aspergillus oryzae or Aspergillus candidus to start the digestion of proteins, fats and carbohydrates. This step is followed by a mixed lactic acid bacteria/alcoholic yeast fermentation, including Zygosaccharomyces rouxii. The set also produces vitamins, antioxidants and flavors. Soy sauce is obtained by a similar process. Boiled soybeans are mixed with roasted wheat kernels and seeded with fungi like Aspergillus oryzae or Aspergillus sojae. Salt or brine is then added. The mixture is filtered and inoculated with various bacteria then yeasts including Zygosaccharomyces rouxii and various Candida. Successive fermentations can last several months. The final filtrate is pasteurized before use. Large variations with additions of various products such as mushroom broths or shrimp will give a great wealth of tastes and varied textures. The markets for these products are in the tens of billions of euros annually.

Eukaryotic protists are also used to produce agents added to foods to improve flavor or texture. These include alginates, agar and carrageenans produced by various algae to gel ice creams or creams (Table 12) or citric acid used to acidify candy. The food industry consumes 1.6 million tonnes of citric acid produced mainly with Aspergillus niger, an Eurotiomycetes Ascomycota.

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