4 State of the World’s Fungi State of the World’s Fungi 2018 4. Useful fungi Thomas Prescotta, Joanne Wongb, Barry Panaretouc, Eric Boad, Angela Bonda, Shaheenara Chowdhurya, Lee Daviesa, Lars Østergaarde a Royal Botanic Gardens, Kew, UK; b Novartis Institutes for BioMedical Research, Switzerland; c King’s College London, UK; d University of Aberdeen, UK; e Novozymes A/S, Denmark 24 Positive interactions and insights USEFUL FUNGI the global market for edible mushrooms is estimated to be worth US$42 billion Per year What makes a species of fungus economically valuable? What daily products utilise fungi and what are the useful fungi of the future for food, medicines and fungal enzymes? stateoftheworldsfungi.org/2018/useful-fungi.html Useful fungi 25 26 Positive interactions and insights (Amanita spp.) and boletes (Boletus spp.)[2]. Most wild- FUNGI ARE A SOURCE OF NUTRITIOUS collected species cannot be cultivated because of complex FOOD, LIFESAVING MEDICINES AND nutritional dependencies (they depend on living plants to grow), whereas cultivated species have been selected to ENZYMES FOR BIOTECHNOLOGY. feed on dead organic matter, which makes them easier to grow in large quantities[2,3]. The rise of the suite of cultivated Most people would be able to name a few species of edible mushrooms seen on supermarket shelves today, including mushrooms but how many are aware of the full diversity of button mushrooms (Agaricus bisporus), began relatively edible species in nature, still less the enormous contribution recently in the 1960s[3]. The majority of these cultivated fungi have made to pharmaceuticals and biotechnology? mushrooms (85%) come from just five genera: Lentinula, In fact, the co-opting of fungi for the production of wine and Pleurotus, Auricularia, Agaricus and Flammulina[4] (see leavened bread possibly marks the point where humans Figure 2). first learned to use the natural world to perform useful Fungi also play a pivotal role in the production of food and chemical reactions. It is part of a story that continues into drinks. Brewer’s or baker’s yeast, Saccharomyces cerevisiae, the present day – the notion of fungi as factories that can underpins almost all bread and alcoholic drink production produce valuable chemical compounds is the bedrock of and is a key ingredient in MarmiteTM and VegemiteTM. The modern biotechnology. In this chapter, we look specifically at meat substitute QuornTM is also manufactured using a fungus edible fungi, medicines and enzymes and draw out the major (Fusarium venenatum), in carefully controlled fermentation applications that provide significant societal benefits. Other vessels that yield 300 kg of the fungus per hour[5]. Fungi significant uses and applications not covered in this chapter are also essential to the production of some types of are summarised in Table 1. cheese, with moulds such as Penicillium camemberti and P. roqueforti used to ripen and give flavour to the cheese. While these two species can be found in many types of EDIBLE FUNGI cheese, the wider diversity of fungi involved is currently The global market for edible mushrooms unknown[6]. Furthermore, the type of cheese produced is is estimated to be worth US$42 billion per not necessarily dependent on the species involved. A DNA year[1]. At least 350 species of fungi are collected and eaten analysis of 44 types of cheese revealed that aside from as food, although the exact number is likely to be higher P. roqueforti, which is specific to blue-veined cheese, there as this information is not available for many countries[2]. was little correlation between the fungal species detected These edible species come from just 18 orders of fungi, and the type of cheese[7]. Interestingly, analysis of a collection which is a small fraction of total fungal diversity (see Figure of P. roqueforti from 120 different blue-veined cheeses found 1). Among wild-collected fungi, the species most commonly distinct populations of the fungus that corresponded to the consumed and traded are brittlegills (Russula spp.), milkcaps different cheese varieties[8], so cheese production appears (Lactarius spp.), chanterelles (Cantharellus spp.), agarics to have shaped the population structure of this species[9]. 350 15% At least 350 species 15% of all vaccines Fungi are being used are consumed as foods and therapeutic proteins to turn crop waste are made in yeast into bioethanol C5H6O4 216 216 species of fungi Itaconic acid from are thought to fungi is used to be hallucinogenic make Lego® Useful fungi 27 TABLE 1: AN OVERVIEW OF THE HUMAN APPLICATIONS OF FUNGI AGRICULTURE Species of Trichoderma are used to enhance the growth of crops and as a source of enzymes added to improve animal feeds[49,50]. Fungi are also the source of an important class of agricultural fungicides called strobilurins[51]. Aspergillus flavus is used as a biocontrol agent on peanut crops to out-compete aflatoxin-producing fungi[52]. BEVERAGES Yeasts underpin alcoholic drink production from beer to wine to spirits. Soft drinks contain citric acid that is produced from the fermentation of Aspergillus niger[53]. Glucoamylase from species of Aspergillus is used to convert starch to high-fructose corn syrup, which is used as a sweetener in soft drinks[54]. BIOFUELS Second-generation bioethanol makes use of species of Trichoderma to break down agricultural waste such as maize straw into sugars that can be fermented using yeast to produce ethanol[42]. BIOREMEDIATION White rot fungi, including Pleurotus ostreatus and Trametes versicolor, can degrade toxic polychlorinated biphenyl (PCB) chemicals in soil and polluted wastewaters[55,56]. COTTON Catalase enzymes from species of Aspergillus are used to break down excess bleach in the wastewater from PROCESSING cotton processing[57]. Trichoderma cellulases are used to remove fine cotton threads, which prevents the fibre aggregating into pills[57]. FOOD At least 350 edible mushroom species are known to be collected for food[2]. The meat substitute QuornTM is manufactured using a fungus (Fusarium venenatum)[5]. Moulds such as Penicillium camemberti and P. roqueforti are integral to the ripening process in many types of cheese[6]. Live yeast and fungal enzymes are used in breadmaking[58]. The food colourings lycopene and beta-carotene are now produced from the fungus Blakeslea trispora[59]. Soy sauce is produced using koji (Aspergillus oryzae) and the Asian snack tempeh makes use of Rhizopus microsporus[60,61]. HALLUCINOGENS Worldwide, 216 species of fungi are believed to be hallucinogenic – of these, 116 species belong to the genus Psilocybe[62]. LEATHER Leather hides are degreased with lipase enzymes from Aspergillus oryzae[63,64]. PROCESSING MEDICINES Many drugs come from fungi. Penicillin from Penicillium rubens revolutionised the treatment of bacterial infections and cyclosporine from Tolypocladium inflatum made organ transplantation possible[11–13]. Gestodene is an active ingredient in third-generation contraceptive pills; a key step in its synthesis is achieved using fungal fermentation with Penicillium raistrickii[65]. PAPER Cellulase enzymes produced by species of Trichoderma and Humicola are used to speed up the pulping process MANUFACTURING thereby reducing water usage[37,38]. PLASTICS AND Plastic car parts, synthetic rubber and LegoTM are made using itaconic acid derived from species of BIOMATERIALS Aspergillus[66,67]. Additionally, fungal mycelium-based products are now being used as replacements for polystyrene foam, leather and building materials[68–70]. RESEARCH Since 2010, more than a quarter of Nobel prizes for physiology or medicine were awarded for work based on yeast[71]. VITAMINS The vitamin B2 used for vitamin supplements is produced by fermentation of the fungus Eremothecium gossypii[72]. WASHING Cellulase enzymes produced by the thermophilic fungus Humicola insolens are added to washing powders and DETERGENTS liquids. They trim the fine cotton threads on the surface of cotton fabric to produce a smoother, newer feel[41,73]. Lipase enzymes from the same species are also added to break down fat stains[40,41]. As is the case for other areas of mycology, identifying and FUNGAL PHARMACEUTICALS naming species of edible mushrooms can be problematic. Fungi have made major contributions to the For example, in a study conducted at Kew, DNA was world of medicine. For example, penicillin from extracted from a packet of dried porcini mushrooms bought the fungus Penicillium rubens revolutionised the treatment from a shop in London. Analysis of the DNA revealed that of bacterial infections, while cyclosporine from the fungus rather than being from a single known species (Boletus Tolypocladium inflatum made organ transplantation possible edulis), the chopped pieces of mushroom in the packet by helping to prevent rejection of the donated organs[11–13]. came from three different species, each of which was new Other notable examples include the cholesterol-lowering to science[10]. This demonstrates that not only do we eat drug lovastatin, from Aspergillus terreus, and fingolimod, just a small fraction of the edible mushrooms available which is used to treat multiple sclerosis (see Figure 3). in nature, we can’t even be sure of the identity of those The chemical structure of fingolimod took inspiration from that we do eat! myriocin, a chemical compound produced by Isaria sinclairii. 28 Positive interactions and insights FIGURE 1: EDIBLE FUNGAL DIVERSITY IN COMPARISON TO TOTAL FUNGAL DIVERSITY The fungi that are recorded as being eaten for food