Amanita bisporigera

Taxonomy

Amanita bisporigera was first described scientifically in 1906 by American botanist George Francis Atkinson in a publication by Cornell University colleague Charles E. Lewis. The type locality was Ithaca, New York, where several collections were made. In his 1941 monograph of world Amanita species, Édouard-Jean Gilbert transferred the species to his new genus Amanitina, but this genus is now considered synonymous with Amanita. In 1944, William Murrill described the species Amanita vernella, collected from Gainesville, Florida; that species is now thought to be synonymous with A. bisporigera after a 1979 examination of its type material revealed basidia that were mostly 2-spored. Amanita phalloides var. striatula, a poorly known taxon originally described from the United States in 1902 by Charles Horton Peck, is considered by Amanita authority Rodham Tulloss to be synonymous with A. bisporigera. Vernacular names for the mushroom include "destroying angel", "deadly amanita", "white death cap", "angel of death" and "eastern North American destroying angel".

Amanita bisporigera belongs to section Phalloideae of the genus Amanita, which contains some of the deadliest Amanita species, including A. phalloides and A. virosa. This classification has been upheld with phylogenetic analyses, which demonstrate that the toxin-producing members of section Phalloideae form a clade—that is, they derive from a common ancestor. In 2005, Zhang and colleagues performed a phylogenetic analysis based on the internal transcribed spacer (ITS) sequences of several white-bodied toxic Amanita species, most of which are found in Asia. Their results support a clade containing A. bisporigera, A. subjunquillea var. alba, A. exitialis, and A. virosa. The Guangzhou destroying angel (Amanita exitialis) has two-spored basidia, like A. bisporigera.

Description

The cap is 3-13 cm wide and, depending on its age, ranges in shape from egg-shaped to convex to somewhat flattened. The cap surface is smooth and white, sometimes with a pale tan- or cream-colored tint in the center. The surface is either dry or, when the environment is moist, slightly sticky. The flesh is thin and white, and does not change color when bruised. The margin of the cap, which is rolled inwards in young specimens, does not have striations (grooves), and lacks volval remnants. The gills, also white, are crowded closely together. They are either free from attachment to the stipe or just barely reach it. The lamellulae (short gills that do not extend all the way to the stipe) are numerous, and gradually narrow.

Microscopic features

Genome

The Amanita Genome Project was begun in Jonathan Walton's lab at Michigan State University in 2004 as part of their ongoing studies of A. bisporigera. The purpose of the project is to determine the genes and genetic controls associated with the formation of mycorrhizae, and to elucidate the biochemical mechanisms of toxin production. The genome of A. bisporigera has been sequenced using a combination of automated Sanger sequencing and pyrosequencing, and the genome sequence information is publicly searchable. The sequence data enabled the researchers to identify the genes responsible for amatoxin and phallotoxin biosynthesis, AMA1 and PHA1. The cyclic peptides are synthesized on ribosomes, and require proline-specific peptidases from the prolyl oligopeptidase family for processing.

The genetic sequence information from A. bisporigera has been used to identify molecular polymorphisms in the related A. phalloides. These single-nucleotide polymorphisms may be used as population genetic markers to study phylogeography and population genetics. Sequence information has also been employed to show that A. bisporigera lacks many of the major classes of secreted enzymes that break down the complex polysaccharides of plant cell walls, like cellulose. In contrast, saprobic fungi like Coprinopsis cinerea and Galerina marginata, which break down organic matter to obtain nutrients, have a more complete complement of cell wall-degrading enzymes. Although few ectomycorrhizal fungi have yet been tested in this way, the authors suggest that the absence of plant cell wall-degrading ability may correlate with the ectomycorrhizal ecological niche.

Similar species

The color and general appearance of A. bisporigera are similar to those of A. verna and A. virosa. A. bisporigera is at times smaller and more slender than either A. verna or A. virosa, but it varies considerably in size; therefore size is not a reliable diagnostic characteristic. A. virosa fruits in autumn—later than A. bisporigera. A. elliptosperma is less common but widely distributed in the southeastern United States, while A. ocreata is found on the West Coast and in the Southwest. Other similar toxic North American species include Amanita magnivelaris, which has a cream-colored, rather thick, felted-submembranous, skirt-like ring, and A. virosiformis, which has elongated spores that are 3.9–4.7 by 11.7–13.4 μm. Neither A. elliptosperma nor A. magnivelaris typically turn yellow with the application of KOH; the KOH reaction of A. virosiformis has not been reported.

Leucoagaricus leucothites is another all-white mushroom with an annulus, free gills, and white spore print, but it lacks a volva and has thick-walled dextrinoid (staining red-brown in Melzer's reagent) egg-shaped spores with a pore. A. bisporigera may also be confused with the larger edible species Agaricus silvicola, the "horse-mushroom". Like many white amanitas, young fruit bodies of A. bisporigera, still enveloped in the universal veil, can be confused with puffball species, but a longitudinal cut of the fruit body reveals internal structures in the Amanita that are absent in puffballs. In 2006, seven members of the Hmong community living in Minnesota were poisoned with A. bisporigera because they had confused it with edible paddy straw mushrooms (Volvariella volvacea) that grow in Southeast Asia.

Habitat and distribution

Like most other Amanita species, A. bisporigera is thought to form mycorrhizal relationships with trees. This is a mutually beneficial relationship where the hyphae of the fungus grow around the roots of trees, enabling the fungus to receive moisture, protection and nutritive byproducts of the tree, and giving the tree greater access to soil nutrients. Fruit bodies of A. bisporigera are found on the ground growing either solitarily, scattered, or in groups in mixed coniferous and deciduous forests; they tend to appear during summer and early fall. The fruit bodies are commonly found near oak, but have been reported in birch-aspen areas in the west. It is most commonly found in eastern North America, and rare in western North America. It is widely distributed in Canada, and its range extends south to Mexico. The species has also been found in Colombia, where it may have been introduced from trees exported for use in pine plantations.

Toxicity

A. bisporigera is considered the most toxic North American Amanita mushroom, with little variation in toxin content between different fruit bodies. Three subtypes of amatoxin have been described: α-, β, and γ-amanitin. The principal amatoxin, α-amanitin, is readily absorbed across the intestine, and 60% of the absorbed toxin is excreted into bile and undergoes enterohepatic circulation; the kidneys clear the remaining 40%. The toxin inhibits the enzyme RNA polymerase II, thereby interfering with DNA transcription, which suppresses RNA production and protein synthesis. This causes cellular necrosis, especially in cells which are initially exposed and have rapid rates of protein synthesis. This process results in severe acute liver dysfunction and, ultimately, liver failure. Amatoxins are not broken down by boiling, freezing, or drying. Roughly 0.2 to 0.4 milligrams of α-amanitin is present in 1 gram of A. bisporigera; the lethal dose in humans is less than 0.1 mg/kg body weight. One mature fruit body can contain 10–12 mg of α-amanitin, enough for a lethal dose. The α-amanitin concentration in the spores is about 17% that of the fruit body tissues. A. bisporigera also contains the phallotoxin phallacidin, structurally related to the amatoxins but considered less poisonous because of poor absorption. Poisonings (from similar white amanitas) have also been reported in domestic animals, including dogs, cats, and cows.

The first reported poisonings resulting in death from the consumption of A. bisporigera were from near San Antonio, Mexico, in 1957, where a rancher, his wife, and three children consumed the fungus; only the man survived. Amanita poisoning is characterized by the following distinct stages: the incubation stage is an asymptomatic period which ranges from 6 to 12 hours after ingestion. In the gastrointestinal stage, about 6 to 16 hours after ingestion, there is onset of abdominal pain, explosive vomiting, and diarrhea for up to 24 hours, which may lead to dehydration, severe electrolyte imbalances, and shock. These early symptoms may be related to other toxins such as phalloidin. In the cytotoxic stage, 24 to 48 hours after ingestion, clinical and biochemical signs of liver damage are observed, but the patient is typically free of gastrointestinal symptoms. The signs of liver dysfunction such as jaundice, hypoglycemia, acidosis, and hemorrhage appear. Later, there is an increase in the levels of prothrombin and blood levels of ammonia, and the signs of hepatic encephalopathy and/or kidney failure appear. The risk factors for mortality that have been reported are age younger than 10 years, short latency period between ingestion and onset of symptoms, severe coagulopathy (blood clotting disorder), severe hyperbilirubinemia (jaundice), and rising serum creatinine levels.

References

Cited books

References

1. Mueller, G.M.. (2025). "''Amanita bisporigera''".
2. {{NGSWG
3. [[Audubon]]. (2023). "Mushrooms of North America". [[Knopf]].
4. Jenkins, 1986, pp. 140–41.
5. (2016-01-01). "Expansion and diversification of the MSDIN family of cyclic peptide genes in the poisonous agarics Amanita phalloides and A. bisporigera". BMC Genomics.
6. Jenkins, 1986, p. 146.
7. Jenkins, 1986, p. 141.
8. Jenkins, 1986, p. 5.
9. (2006). "Primer note: Using the incomplete genome of the ectomycorrhizal fungus ''Amanita bisporigera'' to identify molecular polymorphisms in the related ''Amanita phalloides''". Molecular Ecology Notes.
10. (1985). "Poisonous Mushrooms of Canada: Including other Inedible Fungi". Fitzhenry & Whiteside in cooperation with Agriculture Canada and the Canadian Government Publishing Centre, Supply and Services Canada.
11. (2009). "Mushrooms of the Pacific Northwest: Timber Press Field Guide (Timber Press Field Guides)". Timber Press.
12. Benjamin DR. (1995). "Mushrooms, Poisons and Panaceas. A Handbook for Naturalists, Mycologists, and Physicians". W.H. Freeman.
13. (2010). "Spotlights on advances in mycotoxin research". Applied Microbiology and Biotechnology.
14. Dart RC. (2003). "Medical toxicology". Lippincott, Williams & Wilkins.
15. (1999). "Molecular phylogeny of ''Amanita'' based on large-subunit ribosomal DNA sequences: implications for taxonomy and character evolution". Mycologia.
16. (1996). "Histological criteria for diagnosis of ''Amanita'' poisoning". Journal of Forensic Sciences.
17. Gilbert E-J. (1940). "Amanitaceae". Iconographia Mycologica.
18. Guzmán G.. (1973). "Some distributional relationships between Mexican and United States mycofloras". Mycologia.
19. Hall IR. (2003). "Edible and Poisonous Mushrooms of the World". Timber Press.
20. (2007). "Gene family encoding the major toxins of lethal ''Amanita'' mushrooms". Proceedings of the National Academy of Sciences of the United States of America.
21. Helm R.. (1957). "Sur un cas d'empoisonnement mortel cause au Mexique par l'Amanita bisporigera Atk.". Revue de Mycologie.
22. Jenkins DT. (1979). "A study of ''Amanita'' types III. Taxa described by W. A. Murrill". Mycotaxon.
23. (2008). "Dictionary of the Fungi". CAB International.
24. Lewis CE. (1906). "The basidium of ''Amanita bisporigera''". Botanical Gazette.
25. (2006). "''Amanita bisporigera'' ingestion: mistaken identity, dose-related toxicity, and improvement despite severe hepatotoxicity". Pediatric Emergency Care.
26. (2010). "Amatoxin and phallotoxin concentration in ''Amanita bisporigera'' spores". Mycologia.
27. (2006). "North American Mushrooms: a Field Guide to Edible and Inedible Fungi". Falcon Guide.
28. Murrill WA. (1944). "More fungi from Florida". Lloydia.
29. (2009). "Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus ''Amanita bisporigera'', based on the secretome of ''Trichoderma reesei''". Fungal Genetics and Biology.
30. Peck CH. (1902). "Report of the State Botanist 1901". Bulletin of the New York State Museum.
31. (1994). "Handbook of Mushroom Poisoning: Diagnosis and Treatment". CRC Press.
32. (1980). "The Mushroom Hunter's Field Guide". University of Michigan Press.
33. Tu AT.. (1992). "Food Poisoning". Dekker.
34. (1966). "Occurrence of amanita toxins in American collections of deadly amanitas". Journal of Pharmaceutical Sciences.
35. Kuo M.. (October 2003). "''Amanita bisporigera''". MushroomExpert.Com.
36. Madhok M.. (2007). "''Amanita bisporigera''. Ingestion and death from mistaken identity". Minnesota Medicine.
37. "''Amanitina bisporigera'' (G.F. Atk.) E.-J. Gilbert 1941". [[MycoBank]]. International Mycological Association.
38. Tulloss R. "''Amanita bisporigera'' G. F. Atk.". Amanita studies.
39. Tulloss R.. (2009). "''Amanita magnivelaris'' Peck". Amanita studies.
40. "The ''Amanita'' Genome Project: Scientific Importance". Michigan State University.
41. Tullos R. "''Amanita elliptosperma'' G.F. Atk., ''A. gwyniana'' Coker, ''A. hygroscopica'' Coker, ''A. parviformis'' (Murrill) Murrill, ''A. pseudoverna'' (Murrill) Murrill, ''A. verniformis'' (Murrill) Murrill". Amanita Studies.
42. (2005-07-16). "Key to Species of AMANITA Section PHALLOIDEAE from North and Central America". Amanita studies.
43. Tulloss R.. "''Amanita magnivelaris'' Peck". Amanita Studies.
44. "BLAST Search". Michigan State University DOE Plant Research Laboratory and the Bioinformatics Core of the Research Technology Support Facility at MSU.
45. (1998). "Molecular phylogenetic studies in the genus ''Amanita''". Canadian Journal of Botany.
46. (2005). "Production and characterization of Amanitin toxins from a pure culture of ''Amanita exitialis''". FEMS Microbiology Letters.
47. (2010?). "Enhanced detection of toxic peptides from ''Amanita bisporigera'' mushrooms". FASEB Journal.