I was interested to read about some people in Rwanda who eat large quantities of a mushroom from the genus Amanita that grow in the Eucalyptus plantations there. This mushroom is called Amanita bweyeyensis. There is a YouTube video on the subject, from which this image is clipped.
https://www.youtube.com/watch?v=PtjRvTmg3GY
This mushroom sits within the Phalloideae section of Amanita, where the deadly species containing amatoxins reside. Despite this, it does not contain amatoxins nor phallotoxins. It is the amatoxins that are the cause of many fatalities when people eat other mushrooms in this section such as Amanita phalloides. Phallotoxins are not orally active so pose less of a threat.
DNA analysis shows that this mushroom sits within a small cluster that includes the white “death cap” mushrooms from Western Australia. These are: A. djarilmari, A. eucalypti, A. gardneri and A. marmorata. The partial phylogenetic tree is from this paper: https://mycokeys.pensoft.net/article/34560/zoom/fig/11/
Analysis of the Western Australian species has shown that these do not contain amatoxins either. This is reported in a paper that is behind a paywall but the precis is shown at this link. It i available on Deepdyve to which I have a subscription. I have also tested two of them myself using a RAT style test kit as well as thin layer chromatography and have not been able to detect amatoxins.
This is a picture of the Amanita bweyeyensis from the paper mentioned above.
The images below show two of the white species from WA as well as Amanita millsii collected from Tasmania.
These species are quite close in morphology and genetically. It requires multi-locus analysis to separate them on DNA analysis. There are some small differences in spore shape, with Amanita millsii having almost spherical spores. The undescribed species in the herbarium collection are similarly close genetically.
Since the African species sit so close to the WA species in terms of genetics and they grow in Eucalyptus plantations, it is tempting to think that they might have their origins in WA. If this is the case, they do not seem to have been recorded here. It is hard to know where the Eucalyptus trees planted in Rwanda came from originally; they are not WA natives but it is not beyond the realms of possibility that they came from Western Australia, given that this is the closest state to Africa.
This brings to mind the green Russulas that grow in the Eucalypt plantations in Madagascar which are eaten by the people there. They also peel those mushrooms before consumption. These Russulas are unknown in Australia though it would seem likely that is their origin.
How are amatoxins produced?
The production of amatoxins has been investigated in some detail by Heather Hallen and others in terms of genes. It has been shown that the amatoxins originate from proproteins synthesised on the ribosome. The function of the ribosome is shown in this rather cute image which is by SITNBoston and is taken from the Harvard University Site.
The codon carried on the mRNA (we all know what this is these days!) is decoded in the ribosome and amino acids carried by tRNA are converted into an amino acid chain which is known as a proprotein. This is similar to the process by which the covid spike proteins are produced by the mRNA vaccines.
These proproteins have a size in the range of 34 to 35 amino acids whereas the toxins have a size of 8 amino acids. In order for the amatoxins to be produced, these long chains need to be reduced in size and the fragments cyclised. This process has been studied in the amatoxin-producing genus Galerina by a group of researchers and the process is shown in this image from that publication.
The proproteins are acted on by the prolyl oligopeptidase enzyme which cuts the chain at the Proline amino acid and then stitches together the piece that is clipped out to form the bicyclic polypeptides (2 rings of amino acids) that we know as amatoxins.
The amatoxins are bicyclic (=two rings) octapeptides (=contain 8 peptides) with C-to-N (head-to-tail) condensation of the peptide backbone and a cross-bridge between Tryptamine(Trp) and Cisteine (Cys). Three of the amino acids (Trp, Pro, and Ile) are hydroxylated. Phallotoxins are similar in structure but their macrocycles comprise only seven amino acids. The relationship between the different amino acids is shown more clearly in this labelled diagram.
The image below shows a 3D view of an amatoxinA molecule in a similar orientation to the image above. The yellow sulfur atom can be seen within the structure and the 5-membered nitrogen-containing hetercyclic ring of (hyroxylated) Proline (P) seen on the left hand side with the (hydroxylated) Isoeucine (I) skeleton above it and Asparagine(N) below it. There is also a bridge with the (hyroxylated) Tryptamine sitting in the middle of the structure which is facing out into the page.
This type of structure is very stable and survives heating and the action of digestive enzymes. That is one of the reasons that this type of toxin is so dangerous.
Just why this group of mushrooms does not always produce these toxins doesn’t seem to be well understood. I believe that specimens of Amanita marmorata taken from the same region in Hawaii have tested positive in one case and negative in another. The Hawaiian species however differ quite widely in appearance and show some genetic divergence from the Australian specimens Amanita reidii from South Africa is reported to contain amatoxins and it has been suggested that it is in fact Amanita marmorata but genetic differences put this in doubt.
The origin of this clade is put at around 60 million years ago. There is some suggestion that Amanita millsii might have been separated from the Western Australian species by the dry interior of the country at around 15 million years ago but this whole area of research requires more work and samples.
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