THE REAL NUTRITIONAL VALUE OF FUNGI

by Stephanie Ingram

2002

Fungi have been influencing human affairs for thousands of years, whether as a direct food source, as a medicine, or in a food process. Today food of fungal origin is consumed all over the world in vast quantities, and commercial production is part of a rapidly growing industry.  Fungi are of excellent value nutritionally, and of great importance to vegetarians.  Edible mushrooms have high protein content, and are an excellent source of fibre, vitamins, and some minerals.  Efforts to combat the world’s food shortage, led to the production of ‘single cell protein’, grown in industrial fermenters using yeast cells.  The result is a protein extract with high amino acid content potentially favourable for application to human nutrition.  One particularly successful model was that of myco-protein, marketed as Quorn^Ò.  Essentially the mycelium of Fusarium venenatum, its filamentous nature much resembles the fibres of meat.  Quorn is now available in supermarkets, marketed as a high-protein, low-fat, cholesterol-free ‘meat alternative’.  When it comes to fungi as a food source, many people are apprehensive and much education is needed before the true nutritional value of such a cheap, readily available food source can be fully realised.

1.      INTRODUCTION

1.1.      Use of fungi in human affairs

Fungi have a profound influence on human affairs, and their use in food is a very ancient practice.  Greek consumption may have begun as early as the fifth century BC where records in the classical writings of Hippocrates and Euripides mention fungus poisoning.  During the years of the Roman Empire, the death of the emperor Claudius was said to be due to the eating of a plate of poisoned mushrooms.  Some of the fungi were even regarded as great luxuries with magical properties, considered food of the gods.

The cultivation of macrofungi to yield fruit bodies began to flourish in the beginning of the seventeenth century, and today over six million tonnes of edible mushrooms are produced commercially each year around the world.

Many fungi are of considerable medical significance.  For thousands of years, Eastern cultures have revered mushrooms as both food and medicine.  Mushrooms or their extracts are made into a soup or tea, research suggesting they may aid in the treatment of certain types of cancer, boost the immune system and reduce the risk of coronary heart disease.

Other fungi are used to modify food to make it more nutritious or palatable.  Tuber melanosporum, known to most as the truffle, has a taste and aroma so intense that it is used as flavouring instead of a separate dish.  Soy sauce is also produced by growing a filamentous fungus on Soya beans.  It is used extensively as a flavouring and condiment in Chinese cuisine.

Yeast cells and mould mycelium (known collectively as ‘single-cell protein’) grown in fermenters are widely used as nourishment.  Modern developments include a novel food termed ‘Quorn’ - mycelium of the fungus Fusarium venenatum grown in fermenter vessels.  The product compares favourably with meat and is the one significant product to have emerged from the efforts to produce ‘single-cell protein’ to combat the world’s food shortage. 

Another use includes the introduction of Penicillium roqueforti into curds of cheese, producing the highly flavoured blue-vein cheeses.

Not only are fungi used as food, but they are also employed in food processes traced back to the times of the Ancient Egyptians.  Saccharomyces cerevisiae, a yeast, is used in the production of ethanol: when added to glucose solution (or ‘wort’) in anaerobic conditions it will ferment sugars into beer.  Another product of fermentation, carbon dioxide, is exploited in the bread making industry, where it leads to a well-risen loaf.

1.2.      Nutritional value

Today food of fungal origin is consumed all over the world in vast quantities, and commercial production is part of a rapidly growing industry.  From mushroom farmers to Quorn-makers, there are plenty of people anxious to sell you fungus as food, usually with a claim that their product represents healthy eating.  But how far can these claims be justified?

Ancient cultures believed edible fungi promoted healthiness and well-being.  These people may have been right, but not because fungi share magical characteristics.  Fungi are of excellent nutritional importance and deserve attention for their unique contributions to a healthy diet.

2.      MUSHROOMS AND MACROFUNGI

2.1.           Cultivation

The word ‘mushroom’ is thought to have been derived from the French ‘mousseron’, a term that included edible mushrooms as well as poisonous varieties.  Today, the word refers only to edible fungi, and is generally applied to the above-ground portion, the fruiting body.  Those without the typical stem and cap are identified by their specific names such as morels or truffles.

Mushrooms have played an important role in the diet of many people for thousands of years.  Ancient Egyptian hieroglyphics reveal that mushrooms were thought to bring immortality.  Many later cultures believed that eating mushrooms could endow them with super-human strength, give them clairvoyance in locating lost objects and lead the soul to reside with the gods.

The cultivation of mushrooms in Europe has been going on for nearly 300 years.  It began in the underground caves of Paris in the time of Louis XIV and flourished until the mid-twentieth century.  Mushrooms are now being produced in over eighty countries around the world.  In 1945, the British Mushroom Grower’s Association (MGA) was born and total production was estimated at some 450 tonnes.  Today total annual production is estimated at over six million tonnes.  Britain is the fourth largest producer being surpassed only by the USA, France and Taiwan.

In various countries in Asia, up to eighty distinct varieties of wild fungi are offered for sale in the markets.  In Britain, the public are much more apprehensive when it comes to buying wild mushrooms.  Even so, it is perhaps remarkable that success on a large scale has been achieved with the commercial production of a very few.

2.2.           Cultivated Species

Agaricus bisporus

Known also as the white or button mushroom, this is the most commonly cultivated in Britain.  It varies in colour from creamy white to light brown and in sizes from small (button) to jumbo.  They are pleasingly mild and woodsy, their flavour intensifying when cooked.  They were first cultivated on prepared horse manure in seventeenth century France, and in caves that provided the ideal stable environment in terms of temperature and humidity.  Today they are strictly cultivated in rich compost in purpose-built mushroom houses where heat and humidity are carefully controlled – it being the most technically advanced horticultural industry as a result.

Lentinula edodes

More commonly known as Shiitake mushrooms, they have been commercially cultivated since their original importation into Europe from Japan around 1940 and are widely available in supermarkets as well as in Asian markets.  Originally harvested from hardwood trees in their native country for at least two thousand years, they are best cultivated on artificial logs.  Shiitake has a medium brown colour with a distinctive, thick, umbrella-shaped cap, and offer a rich, distinctly earthy flavour and chewy texture.  Introduction of a mushroom more aromatic and flavourful than the common button mushroom has rapidly increased demand.  After Agaricus, Shiitake is the second most cultivated mushroom in the world.  Healthfood stores, oriental and upscale restaurants are all targets for this speciality mushroom. A notable peculiarity, though, is that the mushroom is dried before sale in Asia (and this develops the full flavour), but is sold fresh in Europe.

Other macrofungi in commercial cultivation

Four other mushrooms are grown on a smaller commercial scale.  Pleurotus spp, the oyster mushroom is grown mainly in Central Europe.  A soft brown colour, it is a large mushroom with a shape comparable to that of an oyster shell.  Oyster mushrooms have a delicate, mild flavour and velvety texture.  Volvariella volvacea, the paddy straw mushroom (so-called because its substrate is a compost of rice straw), has been cultivated for 2000 years in China and South-east Asia.  The others are Flammulina velutipes (or enoki) a unique mushroom with a long, slender stem and tiny cap, grown mainly in Japan, and Pholiota nameko, cultivated in China and Taiwan.

Another macrofungus worth mentioning is the truffle.  Sometimes regarded as a mushroom, the truffle is a subterranean European fungus belonging to the order Tuberales with an underground fruiting body, usually round and pitted.  Truffles have been collected for at least 3600 years.  The most highly prized is the black truffle, Tuber melanosporum.  Its tantalizing taste and aroma are so intense that it is used as flavouring instead of a separate dish.

2.3.           Mushrooms and nutrition

Varying opinions have been expressed regarding the true nutritive value of edible mushrooms.  Although mushrooms are a staple food in the diet of some cultures, edible mushrooms are usually considered for their flavour and condiment value.  In the past, authors have dismissed mushrooms as a food of little nutritive value, some considering them devoid of nutrients.  However, this naïve approach is simply inaccurate, as much research conducted on mushrooms suggests otherwise, showing mushrooms as a nutritionally sound food that are of even greater value to vegetarians.

To begin with, mushrooms have a fairly high protein content, typically 20-30% crude protein as a percentage of dry matter.  However there is extreme variation among species (3.5% in Cantharellus cibarius, 44% in Agaricus bisporus).  High protein content makes them an ideal food because they contain all the amino acids essential to human nutrition.  There are about eight essential amino acids, that is, those which cannot be produced by the human body, and so must be consumed in the diet daily.  Mushrooms can be an important dietary source of these amino acids.

Since fats and carbohydrates are rarely lacking in diets typical of the western (developed) world, protein is the most critical component contributing to the nutritional value of a food.  It is therefore the component considered most important in nutritional evaluation.  The amino acid content, specifically the content of essential amino acids is considered a reliable measure of nutritive value.

In 1959, Oser proposed the use of an Essential Amino Acid Index (EAA Index) to rate dietary protein in terms of the ratio of the essential amino acids contained in a food relative to the essential amino acid content of a highly nutritive reference protein, whole egg protein in this case.  On examination of EAA Indexes, although those analysed contained all essential amino acids, every species was limited in their availability of at least one essential amino acid, some in up to seven.  This finding is supported by Anderson and Fellers (1942), who reported that rats given mushrooms as their only source of protein gained only 30% of the weight gained by control animals.  This suggests mushroom protein alone is nutritionally inadequate. 

Agaricus bisporus has values highly comparable to whole egg protein.  It was found that the most nutritive mushrooms rank in potential nutritive value with those calculated for meat and milk, the only difference being relatively low content of certain amino acids, namely isoleucine, leucine, lysine and histidine.  On the other hand, relative levels of lysine and tryptophan were significantly higher than those for legumes and vegetables.  Even the least nutritive mushrooms were comparable to some common vegetables.  Mushroom protein appears to be intermediate in nutritional quality between meat and vegetable proteins.

After moisture, which accounts for 90% of fresh weight, carbohydrates are the main component of mushrooms (average of 4.2%).  Polymeric carbohydrates that occur include glycogen (an energy store compound also found in humans and comparable to starch in plants), and chitin or “fungus cellulose”, a polymer of N-acetylglycosamine, the structural component of the fungal cell wall.  Chitin is not easily digestible and is considered to be the major constituent of the fibre content.  The cell wall contains many other large carbohydrate polymers such as glucans, chitosans and mannans, and, including chitin, these polymers are linked together with covalent bonds that cannot be attacked by our digestive enzymes.  Therefore, it is suspected that humans cannot utilise a large percentage of the carbohydrate in mushrooms as nutrients and so it functions only as roughage.

Because mushrooms can’t photosynthesise sugars, carbohydrates are present in lower proportions than vegetables such as carrots and sprouts, and so provide only a fraction of the energy requirement.  Mushrooms contain an average of 85-125 kJ per 100 g whereas an adult male needs about 10 000 kJ per day.  This low energy value of mushrooms enables it to be used in low-calorie diets.  The low carbohydrate value makes them an ideal food for diabetics.

Mushrooms are characteristically low in fat, comprising 2-8% dry weight.  This crude fat includes representatives of all classes of lipid compounds including free fatty acids, glycerides, sterols, and phospholipids.  Of existing fatty acids, a high proportion are linoleic acid (the only essential fatty acid required in the human diet), found to be 63-74% of total fatty acids.  Sphingolipids, important in the brain and nervous system, have also been identified, but appear to represent only a small proportion of total glycolipids.

Like vegetables, mushrooms are a cholesterol free food.  This is promising in terms of health issues, as cholesterol is regarded as a risk factor of coronary heart disease and related conditions.  A study carried out by Fukushima et al. (2000) reported that some mushrooms in Basidiomycotina have the ability to lower serum cholesterol concentration.  Using Agaricus bisporus, they found that rats fed a diet of the mushroom fibre led to lowered serum total cholesterol and lowered VLDL, IDL and LDL cholesterol concentrations, all thought to be atherogenic lipoproteins.  Cheung (1998) also described how edible mushrooms are an ideal food for the prevention of atherosclerosis due to their high fibre content.  His study concluded that the inclusion of edible mushrooms into the diet has a hypocholesterolemic effect, perhaps due to dietary fibres such as b-glucans, which may increase intestinal motility, reducing bile acid and cholesterol absorption.

In the kitchen, mushrooms are popularly sautéred, roasted, grilled, broiled or fried in a variety of dishes giving rise to a whole selection of flavours.  All these techniques, however, require the use of butter or oil, ultimately adding to its fatty value, thus increasing the amount of cholesterol consumed.  Mushrooms are also commonly stuffed, again possibly adding to the fat content.  It is therefore too straightforward to state simply that eating mushrooms contributes to a low-cholesterol diet, when clearly its fatty value is dependent upon the cooking method.

There are many essential vitamins required daily in the diet.  The fruit body of a mushroom is an excellent source of B-complex vitamins including riboflavin (B₂) niacin, pantothenic acid, thiamin (B₁) biotin, folate and vitamin B₁₂.  Mushrooms are a particularly rich source of riboflavin.  One portabella mushroom takes care of nearly one-third our daily value.  Vegetarians should also be aware that mushrooms are one of the best plant-based sources of niacin around: 100g of fresh mushrooms provide more than a quarter of the adult daily requirement of this vitamin.

Mushrooms are unique in that they contain Vitamin B₁₂, something that vegetables can't produce at all.  Since B₁₂ is mainly of animal origin, deficiency is commonly associated with vegetarian diets.  Mushrooms were found to contain 0.32-0.65 mg per gram of B₁₂, allowing just 3 g of fresh mushrooms to provide the RDA of this vitamin.  Vegetarians may find this a useful way of getting this important nutrient.

Outila et al. (1999) found that ergocalciferol in mushrooms increased serum 25-hydroxyvitamin D concentrations as effectively as did supplements, allowing mushrooms to be reliably recommended as a natural vitamin D source.  Pro-vitamin D is present in some mushrooms, particularly shiitake, and can be converted to vitamin D by ultraviolet irradiation (sunlight).  Vitamin A is uncommon although several mushrooms contain detectable amounts of pro-vitamin A measured as the b-carotene equivalent.  Most cultivated mushrooms are believed to contain low amounts of the fat-soluble vitamins, K and E, and only a small contribution to the daily requirement of vitamin C. 

In general, mushrooms contain significant quantities of phosphorus, potassium, and copper, Agaricus bisporus being especially high in these minerals.  A serving of white mushrooms has more potassium than a tomato; a portabella mushroom has more than a glass of orange juice. 

104 mg of phosphorus can be supplied by 5 raw button mushrooms.  100 g would also supply more than half the daily requirement of copper.  Mushrooms are also an excellent source of selenium.  Foods of animal origin and grains are sources of selenium, but in produce, only mushrooms are a good source.  This is good news for vegetarians, whose sources of selenium are limited.  A serving of shiitake mushrooms provides about one-third of the recommended daily value for selenium.

With their range of unique flavours, high protein value comparable to meat, and important contribution to the supply of vitamins and minerals in the diet, mushrooms prove to a valuable food source.

3.      SINGLE CELL PROTEIN

3.1             Yeast

As world food supply has worsened over the years, attention has focused on mass cultivation of microorganisms as sources of food.  The dietary component most in short supply is protein.  Single cell protein (SCP) is considered the most promising nonconventional protein source in augmenting the world’s protein shortage.

Many microorganisms are able to utilise cheap sources of nitrogen and abundant carbon sources.  The resulting biomass has a high protein content.  Microbial rates are high; a compact fermenter can produce as much protein as a large area of agricultural land and can operate all year round.  These considerations have led to massive industrial research aimed at production of microbial biomass for human consumption.

Various waste products, including cheese whey, starch, fruit-processing residues, animal waste, and petroleum hydrocarbons, have all been used to produce SCP.  Yeast is an especially important fungus and the most promising source of SCP although its growth is not as rapid as that of bacteria.  A study carried out by Lyutskanov et al. (1989) on the applicability of protein extracts from a strain of Saccharomyces cerevisiae revealed the percentage of essential amino acids lysine and isoleucine were higher than that of soya bean and the chemical score of these amino acids higher than egg protein. 

Protein extracts from yeast, however, always carry the problem of high nucleic acid content, which can cause gout and urinary tract stones.  Successful methods of reduction led to a simultaneous decrease of carbohydrate content.  This is also good news as existing results show allergic reactions are associated with high carbohydrate content of nonconventional protein sources.  Its low nucleic acid and carbohydrate content make it a good candidate for large-scale production of high nutritional quality protein extracts, potentially applicable to human nutrition.  One example could be to increase protein quality of cereal based food products.

3.2             Myco-protein

The scale of the protein shortage problem is so large that its resolution is more a matter of economics rather than new technology.  Any novel microbial protein requiring costly research and development would not be able to compete with cheaper alternatives.

Yet one alternative model in the UK was successful, and emerged as a commercial product.  Once described as a “twenty year overnight success story”, myco-protein, marketed as Quorn^Ò and produced my Marlow Foods Ltd, now decorates the shelves of British supermarkets.  Essentially the mycelium of Fusarium venenatum, myco-protein is grown in continuous culture on food-grade glucose derived from starch as the carbon source.  The resulting product is a filamentous hyphal mass, much resembling a meat-like texture.  The marketing behind Quorn centres on its filamentous structure, claiming that it simulates the fibrous nature, chewiness, and succulence of meat.  The structure also allows the fabrication of products of different textures and forms.

Compared with many bacteria and yeasts, the relatively slow growth rate of most filamentous fungi is a disadvantage for biomass production.  However, the slow growth rate generally leads to a lower nucleic acid content.  Nevertheless the RNA content is still moderately high and so must be reduced by a heat-shock process.  This has substantial economic penalties, as other constituents are also lost during the process, perhaps up to one third of the biomass dry weight.

Nutritionally, mycoprotein shares much of the value of the mushroom.  Its net protein utilisation (NPU) is 75/100, comparable to beef (80) and cows milk (also 75).  When supplemented with 0.2% methionine, NPU is 100 (equal to egg protein).  It has a protein content minimum of 44% and contains adequate proportions of all essential amino acids.  Myco-protein is high in dietary fibre, mainly due to chitin and b-glucans in hyphal walls.  Complementary to beef, it is low in saturated fat, contains no cholesterol, and is of low calorie value.  It is a good source of the B vitamins, biotin (16 mg/100 g), riboflavin, niacin and B₆ (content equivalent to lamb), although lacks in B₁₂.  Myco-protein is also an excellent source of zinc, particularly useful to vegetarians.

Still, the nutritive value does rely much upon what is supplemented to the myco-protein as flavouring in much the same way as the mushroom.  Marlow Foods state that “if ever a conflict exists between optimum taste and maximum nutritional benefit, taste will always have priority”.  For example, where Quorn is the ‘meal centre’ in, say, burgers, added fat maintains the desired succulence and, of course, adds to the fat content and number of calories it yields.  It is therefore important again to say that composition depends more on the product recipe than on the myco-protein itself.

Although myco-protein was originally developed to supplement the world’s protein shortage, by the early eighties when the production techniques had been fully established, and it had been approved for public sale, the predicted global protein shortage had not materialised.  Instead, it was sold in the western world as a high-protein, high-fibre, low-fat, cholesterol-free health food: a ‘meat alternative’, also available to vegetarians.  However Quorn is more expensive than most meat products, suggesting it was to be sold to those who would pay the price for a top-quality health food, not those who couldn’t afford meat.  Here the retail price reflects the perceived value created by marketing and not the actual nutritional value.

The first Quorn retail product was a savoury pie sold by Sainsbury’s in 1985.  It was a traditional product rather than a new one to generate consumer interest rather than create apprehension concerning food of fungal origin.  Today over 35 products are available in the UK and many other countries are now being introduced to this fungal health food (in particular USA in Jan 2002), making it significant as the only human food product to have emerged from the much-heralded SCP revolution.

4.      CONCLUSION

It may hopefully be assumed that decisions about diet will be governed by sound nutritional knowledge.  If it were as easy as identifying those foods of high nutritive value, and the corresponding integration into our diets would follow, then maybe many would eat a more balanced diet.  Such hopes are unfortunately often proved to be groundless, and knowledge in itself is not always effective in motivating our actions.  In reality, underdeveloped countries don’t have the liberty to choose what they eat, and when they do, custom and prejudice usually prevail.  The diet of those living in developed countries, although we don’t like to admit it, is dominated more by taste, palatability and price than nutritional value.

Many people are apprehensive concerning fungi as a food source.  Ignorance has led many to become sceptical concerning a food produced by a microorganism, and the majority are cynical that food of fungal origin can hold any great nutritional importance.  It seems much education is needed before the true nutritional value of such a cheap, readily available food source can be taken advantage of.

References

1.                   Svrček, M.  (1994). Mushrooms, A Magna Field Guide.  Magna Books.

2.                   Lange, M. & Bayard Hora, F.  (1963). Collins Guide to Mushrooms and Toadstools.  Collins.

3.                   Groves, J.W.  (1963). Edible and Poisonous Mushrooms of Canada.  Canada Department of Agriculture.

4.                   Flegg, P.B., Spencer, D.M. & Wood, D.A.  (1985). The Biology and Biotechnology of the Cultivated Mushroom.  John Wiley & Sons, p211-223

5.                   Chang, S.T. & Hayes, W.A.  (1978). The Biology and Cultivation of Edible Mushrooms.  Academic Press, p137-165

6.                   Adams, M.R. & Moss, M.O.  (1995). Food Microbiology.  The Royal Society of Chemistry, p301-302

7.                   Deacon, J.W.  (1980). Modern Mycology (3^rd edition).  Blackwell Science, p63-64

8.                   Carlile, M.J. & Watkinson, S.C.  (1994). The Fungi.  Academic Press, p403-416

9.                   Ingold, C.T. & Hudson, H.J.  (1993). The Biology of Fungi (6^th edition).  Chapman & Hall, p197-206

10.               Birch, G.G., Spencer, M. & Cameron, A.G.  (1972). Food Science.  Pergamon Press, p177-178

11.               Moore, D. & Chiu, S.W.  (2001). “Fungal Products as Food”, eds. Pointing, S.B. and Hyde, K.D. in Bio-Exploitation of Filamentous Fungi, Fungal Diversity Research Series 6: 223-251

12.               Percival, P.S.  Food article excerpted from Texas Cooking. http://www.texascooking.com/features/feb2001pam.htm

13.               Licitra, P. “Fun with Fungi”.  http://desires.com/2.1/Food/Fungi/fungi.html

14.               The Mushroom Council.  “Preparation”.  http://www.mushroomcouncil.com/preparation/prep.html

15.               Fun with Fungi.  “Fungi as Food Sources”.  http://web.singnet.com.sg/~linlj/food.htm

16.        Texas Horticulture Program.  “Mushrooms (Enoki, Pleurotus, Shiitake)”, excerpted from Speciality Vegetables in Texas.  http://aggie-horticulture.tamu.edu/extension/specialty/mush.html

17.        Cooper, M.  (2001). “Festive Fungi”, New Scientist, 22 Dec, vol 172 issue 2322, p65

18.               Vegetarians in Paradise.  “The Humongous Fungus Among Us”.  http://www.vegparadise.com/highestperch34.html

19.               Chilton, J.  “The Health Benefits of Mushrooms”, NAMMEX. http://www.nammex.com/MushroomArticles/healthBenefitMushrooms.html

20.               Meadow Mushrooms Ltd. “Mushrooms and Nutrition”.  http://www.meadowmushrooms.co.nz/mushroomnutrition.htm

21.               The Mushroom Council. “Nutrition”.   http://www.mushroomcouncil.com/nutrition/nutri.html

22.               Marlow Foods Ltd.  (2001).  Quorn.  http://www.quorn.com/uk/index.htm

23.               Trinci, A.P.J.  (1992). Myco-protein: A twenty-year overnight success story. Mycological Research 96: 1-13

24.               Fukushima, M. et al.  (2000). LDL receptor mRNA in rats is increased by dietary mushroom (Agaricus bisporus) fibre and sugar beet fibre.  Journal of Nutrition 130: 2151-2156

25.               Cheung, P.C.K.  (1998). Plasma and hepatic cholesterol levels and faecal neutral sterol excretion are altered in hamsters fed straw mushroom diets.  Journal of Nutrition 128: 1512-1516

26.               Outila, T.A. et al.  (1999). Bioavailability of vitamin D from wild mushrooms (Cantharellus tubaeformis) as measured with a human bioassay.  American Journal of Clinical Nutrition 69: 95-98

27.               Lyutskanov, N. et al. (1990).  Protein extracts for nutritional purposes from fragile strains of Saccharomyces cerevisiae: Reduction of the nucleic acid content and applicability of the protein extracts.  Journal of Basic Microbiology 30: 523-528