Amanita Muscaria: Ecology, Chemistry, Myths

Entry Amanita muscaria: Ecology, Chemistry, Myths Quentin Carboué * and Michel Lopez URD Agro-Biotechnologies Industrielles (ABI), CEBB, AgroParisTech, 51110 Pomacle, France; [email protected] * Correspondence: [email protected] Definition: Amanita muscaria is the most emblematic mushroom in the popular representation. It is an ectomycorrhizal fungus endemic to the cold ecosystems of the northern hemisphere. The basidiocarp contains isoxazoles compounds that have specific actions on the central nervous system, including hallucinations. For this reason, it is considered an important entheogenic mushroom in different cultures whose remnants are still visible in some modern-day European traditions. In Siberian civilizations, it has been consumed for religious and recreational purposes for millennia, as it was the only inebriant in this region. Keywords: Amanita muscaria; ibotenic acid; muscimol; muscarine; ethnomycology 1. Introduction Thanks to its peculiar red cap with white spots, Amanita muscaria (L.) Lam. is the most iconic mushroom in modern-day popular culture. In many languages, its vernacular names are fly agaric and fly amanita. Indeed, steeped in a bowl of milk, it was used to Citation: Carboué, Q.; Lopez, M. catch flies in houses for centuries in Europe due to its ability to attract and intoxicate flies. Amanita muscaria: Ecology, Chemistry, Although considered poisonous when ingested fresh, this mushroom has been consumed Myths. Encyclopedia 2021, 1, 905–914. as edible in many different places, such as Italy and Mexico [1]. Many traditional recipes https://doi.org/10.3390/ involving boiling the mushroom—the water containing most of the water-soluble toxic encyclopedia1030069 compounds is then discarded—are available. In Japan, the mushroom is dried, soaked in brine for 12 weeks, and rinsed in successive washings before being eaten [2]. However, the Academic Editor: Łukasz St˛epień fascination emanating from this mushroom is not recent or limited to culinary purposes; its consumption by humans dates back thousands of years, shaping religious and spiritual Received: 13 July 2021 beliefs, notably in Neolithic Siberian societies. The symbolical appeal exerted by the fly Accepted: 30 August 2021 agaric on our collective imagination is found in numerous representations, myths, and Published: 2 September 2021 legends. Some examples are Lewis Caroll’s Alice’s Adventures in Wonderland, the Super Mario videogames series, and German artist Carsten Höller’s installations. This chapter Publisher’s Note: MDPI stays neutral introduces various aspects of A. muscaria, dealing with its ecology, its chemical composition with regard to jurisdictional claims in and pharmaceutical characteristics, and features of ethnomycology. published maps and institutional affil- iations. 2. Ecological Evolution and Applications A. muscaria is a fungus belonging to the division of the Basidiomycota, the order of the Agaricales, and the family of the Amanitaceae. The diameter of cap of the mushroom usually ranges from 4 to 21 cm, but can reach 50 cm. It is characterized by convex to flat Copyright: © 2021 by the authors. shapes, and has bright red color (Figure1). However, there are different varieties with an Licensee MDPI, Basel, Switzerland. important phenotypic diversity, especially regarding the cap color, e.g., Amanita muscaria This article is an open access article var. guessowii is yellow, and A. muscaria var. flavivolvata and Amanita muscaria var. inzengae distributed under the terms and are orange with yellowish warts. A. muscaria var. alba is entirely white, although it is still conditions of the Creative Commons unclear if it is a variety of its own or a white variant of the variety flavivolvata [3]. As a Attribution (CC BY) license (https:// remnant of the universal veil tissues, the cap is covered with white warts and the stipe has creativecommons.org/licenses/by/ 4.0/). a volva limited to concentric rings [4,5]. Encyclopedia 2021, 1, 905–914. https://doi.org/10.3390/encyclopedia1030069 https://www.mdpi.com/journal/encyclopedia EncyclopediaEncyclopedia 20212021,, 11, FOR PEER REVIEW 9062 FigureFigure 1. 1.Basidiocarps Basidiocarps of A. of muscaria A. muscariaobserved observed in the French in the Prealps French (Alpes-de-Haute-Provence, Prealps (Alpes-de-Haute-Provence, France) (Denis Charret France)©). (Denis Charret ©). The basidiospores are released from the basidia during the fruiting season, usually afterThe a rain basidiospores episode [6,7 ].are It isreleased an ectomycorrhizal from the basidia fungus during and itthe is usuallyfruiting associatedseason, usually with Angiospermaeafter a rain episodetrees, such [6,7]. as ItBetula is an ,ectomycorrhizalCastanea, Cistus, andfungusQuercus and itspecies, is usually and associated also coniferous with ones,Angiospermae such as trees,Abies, suchPicea as, and BetulaPinus, Castanea[5,8]. For, Cistus this, reason,and Quercus on this species, day, it and is impossible also conifer- to A. muscaria growous ones, such asbasidiocarps Abies, Picea, and in a laboratory,Pinus [5,8]. althoughFor this reason, it is possible on this to day, grow it myceliumis impossible on synthetic media, despite a very slow growth rate [9]. A comparative genome analysis of the to grow A. muscaria basidiocarps in a laboratory, although it is possible to grow mycelium mitochondrial DNA suggested a common origin of the ectomycorrhizal Amanita, forming a on synthetic media, despite a very slow growth rate [9]. A comparative genome analysis distinct clade from the saprophyte and, therefore, non-symbiotic Amanita [10]. A. muscaria of the mitochondrial DNA suggested a common origin of the ectomycorrhizal Amanita, is adapted to the temperate and boreal regions of the northern hemisphere. Grown on forming a distinct clade from the saprophyte and, therefore, non-symbiotic Amanita [10]. synthetic media, temperature ranging from 11 to 23 ◦C had no effect on the mushroom’s A. muscaria is adapted to the temperate and boreal regions of the northern hemisphere. respiratory activity [11]. A. muscaria usually grows in podzolic soils from deciduous and Grown on synthetic media, temperature ranging from 11 to 23 °C had no effect on the coniferous forests [12]. In these acidic soil conditions, rates of nitrogen mineralization of mushroom’s respiratory activity [11]. A. muscaria usually grows in podzolic soils from the leaf litter by bacteria are low, and nitrogen is mostly present under its poorly mobile deciduous and coniferous forests [12]. In these acidic soil conditions, rates of nitrogen ammonium and organic forms. A. muscaria possesses a high-affinity ammonium importer mineralization of the leaf litter by bacteria are low, and nitrogen is mostly present under gene and, through the mycorrhizal symbiosis, is therefore essential in the plant nitrogen its poorly mobile ammonium and organic forms. A. muscaria possesses a high-affinity am- uptake in such ecosystems [13]. Phylogenetic studies indicate the existence of three distinct geographicalmonium importer clades gene (the and, “Eurasian”, through “Eurasian-Alpine”,the mycorrhizal symbiosis, and “North is therefore American” essential groups) in thatthe plant evolved nitrogen from anuptake ancestral in suchA. muscaria ecosystemspopulation [13]. Phylogenetic located in the studies unglaciated indicate soils the ofexist- the Siberian–Beringianence of three distinct region—connecting geographical clades Eurasia (the “Eurasian”, and America—during “Eurasian-Alpine”, the Neogene and “North period. ThisAmerican” population groups) later that underwent evolved fragmentation from an ancestral during A. itsmuscaria expansion population on the lands located [14]. in This the classificationunglaciated soils may of evolve the Siberian–Beringian as new comparative region—connecting genomic studies areEurasia carried and out America— [15]. The mushroomduring the hasNeogene also been period. reported This population in the southern later hemisphere,underwent fragmentation usually as an accidentalduring its consequenceexpansion on of the the lands introduction [14]. This of classification non-nativetrees may inevolve Chile, as South new comparative Africa, New Zealand,genomic andstudies Australia are carried [16– 19out]. [15]. In Colombia, The mushroom where has it was also introduced been reported through in the planting southern of hemi- non- nativesphere, trees usually in an as effortan accidental to mitigate consequence deforestation, of the it hasintroduction spread to of form non-native new symbiotic trees in interactionsChile, South with Africa, native New trees Zealand, [20]. and Australia [16–19]. In Colombia, where it was in- troducedFungal through nutrition planting is carried of non-native out by absorbotrophy, trees in an effort meaning to mitigate the deforestation, mycelium absorbs it has andspread internalizes to form new in its symbiotic cells the interactions nutrients present with native in the trees surrounding [20]. aqueous film [21,22]. MushroomFungal composition nutrition is carried regarding out aminoby absorbotrophy, acids and sugars meaning is, therefore, the mycelium influenced absorbs by and the typeinternalizes of topsoil in the its myceliumcells the isnutrients growing present in [23]. Thisin the mode surrounding of nutrition aqueous also naturally film [21,22]. allows theMushroom mushrooms composition to accumulate regarding recalcitrant amino acids compounds—especially and sugars is, therefore, heavy influenced metals—in by their the internaltype

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