Why is the Death Cap mushroom so deadly?
On New Year’s Day I visited a favorite, and normally productive, chanterelle patch outside San Luis Obispo to discover an enormous fruiting of the dangerously toxic death cap mushroom (Amanita phalloides).
My culinary disappointment was tempered by my growing fascination with the question, “Why are mushrooms deadly poisonous?” Proximally, the answer is direct: because they contain a peptide, alpha-amanitin, which halts RNA transcription in the cell nucleus. In broader context, the question should be rephrased, “What ecological advantage and evolutionary fitness does the presence of this toxin contribute?”
Amanita phalloides is a newcomer to California. It is known to be a native of Europe, and its first verified collection in California dates to 1938. Anecdotally, its introduction is ascribed to an accidental arrival on the roots of cork oak trees. It is now known from Southern California to British Columbia. A similar introduction (on the roots of Italian chestnuts?) affects the East Coast.
Death cap is an ectomycorrhizal symbiont. This means it forms connections on the root-tips of forest trees; in California, its typical (but not exclusive) partner is coast live oak. Unlike many symbionts which are highly host specific, death cap is promiscuous in its associations as it spreads worldwide. It is now present in South Africa, Australia and most other similar climes.
Ectomycorrhizal (EC) fungi collect major nutrients, nitrogen and phosphorous, and exchange these with the host tree for sugars. Delicate hyphal strands extend outward from the root tip mass into the surrounding soil and mulch. EC also allows efficient active transfer of macronutrients, micronutrients, and soil water to the tree. The chronic phosphorous limitation in serpentine soils makes the EC symbiosis especially important for local forest types on this soil. Studies in Norway discovered up to 50% of a birch tree’s sugar is exchanged at the root tips with EC symbionts.
Other studies describe how a mushroom, Laccaria bicolor, lures springtail insects (Folsoma candida) into traps, consumes them, and transfers the nitrogen obtained to its host tree.
Trees form non-exclusive associations with many fungi. Studies at Pt. Reyes show more than 15 taxa of EC fungi present at the root tips of coast live oak from a single grove. Most of the live oak symbionts are not deadly or even dangerous, and include the sought after chanterelles.
It is an entirely open research question as to whether the recent invasion of Amanita phalloides into the California oak forest is supplanting native fungi. Studies (in Bishop pine) have shown that EC fungi partition their habitat niches very precisely, allowing multiple fungi to coexist in close proximity. I have visited the particular chanterelle patch since the 1970’s without noticing the Aman5.0ita, so the 2012 fruiting might possibly represent a replacement of one symbiont for another, or just be a fortuitous fruiting of an established co-dominant.
The “competitive exclusion principle” argues that if these organisms are competing within the same precise niche, the most successful will replace all others. The deadly toxin of Amanita’s is alpha-amanitin. This is a heat-stable cyclic peptide that interferes with the transcription function of RNA in the nucleus of cells of virtually all organisms.
Humans, dogs, rabbits, and guinea pigs are equally poisoned. The toxic crisis is caused by irreversible liver or kidney damage, as the molecule concentrates in those organs. More expansively: organisms other than bacteria are affected by alpha-amanitin. Insects, worms, flowering plants, and even viroids (infectious single strands of RNA) that cause “mad cow” and disease in plants cannot replicate when treated with amanitin.
Amanitin is a large, very stable molecule (C39H54N10O14S) so it represents a significant metabolic cost to the fungus to create. Several, widely unrelated, taxa of gilled mushrooms possess amanitin toxin, so its synthesis has been separately evolved several times in fungi –supporting the assumption this represents an important competitive innovation for the species. Fortunately, amanitin is too large to cross the blood/brain barrier, so even victims with irreversible liver and kidney damage due to mushroom poisoning are not affected mentally.
An evolutionary entomologist working in New York State, John Jaenike, has discovered four species of mushroom flies in the genus Drosophila that lay eggs in the gills of fruiting Amanita phalloides. The fruit fly taxa are related to ones that inhabit rotting skunk cabbage, but in New England have recently transferred to the recently introduced Amanita fruitings.
Jaenike discovered that Amanita phalloides is toxic to the damaging parasitic nematodes Howardula that reproduce in the stomach of fruit flies. The toxicity of the death cap to the parasitic nematodes results in much greater egglaying (fecundity) by the fruit flies. The fruit flies are affected by the toxic amanitin, especially the males, but the poison is more than offset by the increase in reproduction.
Janike also discovered that most other insects using mushrooms as egg laying sites (craneflies and forest gnats) shun use of the Amanita (due to its toxicity).
Fruiting mushrooms are a scarce and erratically scattered resource for reproduction and larval feeding. Fruiting mushrooms are fully and completely consumed by mushroom gnat larvae, and Jaenike postulates fierce competition for insect breeding sites. Jaenike has published several papers describing the Amanita-Drosophila-Howardula food web. Mushroom flies secured a niche free of competition by exchanging an evolved tolerance to sub-lethal poisoning for escape from nematode parasitism. The increased fitness leads to greater egg-laying ability, and has provided the evolutionary inertia for this recent adaptation.
Nematodes are significant pests of commercial mushroom production, epidemic infestation can result in the loss of the growing beds. The oyster mushroom, Pleurotus osteraceus, traps and consumes nematodes in noose-like knots of hyphal tissue.
So why are Amanita so poisonous? It is an unlikely deterrence to vertebrate predation of the fruiting caps, as the effect is slow-acting (36-72 hours before the toxic crisis in humans) and the toxin is not concentrated in the cap. Evidence supports the hypothesis that the fitness obtained from synthesizing the toxin is secured within the hyphal network. Perhaps toxic Amanita obtain nitrogen from poisoned nematodes, or protect themselves (and their symbiont hosts) from plant parasitic nematode predation.
Perhaps the toxin suppresses the growth of competing fungal webs. It seems clear the toxic effect of death cap is intrinsic to its invasive success worldwide.
Jaenike, J., “Parasite Pressure and the Evolution of Amanitin Tolerance in Drosophila,” Evolution,Vol. 39, No. 6 (Nov., 1985), pp. 1295-1301. Jaenike, J. and T J. C. Anderson, “Dynamics of Host-Parasite Interactions: The Drosophila-Howardula System,” Oikos Vol. 64, No. 3 (Sep., 1992), pp. 533-540. http://web.uvic.ca/~stevep/pdfs/AmNat_02.pdf
Pringle, Anne, and Else Vellinga, “Last chance to know? Using literature to explore the biogeography and invasion biology of the death cap mushroom Amanita phalloides.” http://www.msi.harvard.edu/downloads/teacherworkshop/Readings/Ben_Papers%20_TWS/Pringle%20and%20Vellinga%202006.pdf
Pringle, Anne, Rachel I. Adams, Hugh B. Cross, and Thomas D. Bruns, “The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America,” Molecular Ecology (2009). http://arnarb.harvard.edu/faculty/pringle/pubs/Pringle_MolEcol_2009.pdf
Wolfe, Benjamin E., Franck Richard, Hugh B. Cross, and Anne Pringle, “Distribution and abundance of the introduced ectomycorrhizal fungus Amanita phalloides in North America,” New Phytologist (2009). http://www.oeb.harvard.edu/faculty/pringle/documents/Wolfe_Ap_Distribution.pdf
Wieland, Theodor and H. Faulstich. Amatoxins, Phallotoxins, Phallolysin, and Antamanide: The biologically Active Components of Poisonous Amanita Mushrooms. http://informahealthcare.com/doi/pdf/10.3109/10409237809149870
Horton, Thomas R., and Thomas D. Bruns, “The molecular revolution in ectomycorrhizal ecology: peeking into the black-box,” Molecular Ecology (2001)10, 1855–1871. http://www.cnr.berkeley.edu/brunslab/papers/