Ecology and Evolution of the Amanita Cyclic Peptide Toxins

Abstract

Organisms adapt to their environments by the process of natural selection. Whereas abiotic factors such as temperature and water are relatively stable or periodic, the environment created by other organisms is unstable because they themselves are evolving. The coevolution of organisms locked in antagonistic relationships with each other, often referred to as an “evolutionary arms race,” can lead to rapid and dramatic changes in the genomes and phenotypes of organisms on both sides of the interaction. (Antagonist is used in the sense of “other living things that work to make life difficult” [Dawkins R (1986) The blind watchmaker. WW Norton & Co, New York]). Although traits such as mimicry, camouflage, and running speed in animals usually receive the most attention as exemplars of the power of the arms race to generate the “organized complexity of the living world” (Dawkins R (1986) The blind watchmaker. WW Norton & Co, New York), arguably the most dramatic manifestation of the arms race in some taxa, especially fungi, bacteria, and plants, is their phenomenal skill at chemical synthesis. Collectively, these groups of organisms can biosynthesize tens of thousands of small molecules with highly ornate structures including precise regio- and stereochemistry. To a biochemist, the myriad chemical reactions catalyzed by enzymes are as awe-inspiring as an eagle’s eye or a cheetah’s speed. (And, of course, the phenomenal properties of eyes and muscles are based on enzyme-catalyzed chemical rections). Like those macroscopic animal traits, the chemical richness of the natural world arises in large part from the perpetual struggle for survival between bacteria, fungi, and plants with each other and with their animal antagonists. It is from this perspective that we will consider the ecological function of the Amanita cyclic peptide toxins.

Miss G. Lister in a letter in September, 1916, wrote: “I have watched a squirrel eating a Tricholoma, I think it may have been terreum…a very pretty sight. I have also watched a rabbit eating Amanita rubescens in our forest, while we were waiting for badgers in the dusk.”

(Hastings and Mottram 1916)