Not all bad: Synopsis of our publication on the distribution of gyromitrin in Discinaceae

Background

Earlier this year, myself and collaborators published an article in the journal Mycologia entitled “Not all bad: Gyromitrin has a limited distribution in the false morels as determined by a new ultra high-performance liquid chromatography method” (Dirks et al. 2023), the findings of which are summarized here.

​Gyromitrin is a mycotoxin found in some false morels, also known as lorchels (mushrooms in the genus Gyromitra), and is highly toxic. However, methods exist to process toxic lorchels (particularly Gyromitra esculenta) to rid the mushrooms of most of their gyromitrin, allowing them to be eaten without acute illness. People rave about the taste of these mushrooms.

In North America, Gyromitra brunnea, Gyromitra caroliniana, Gyromitra korfii, and Gyromitra montana are commonly consumed without special preparation, but not without controversy. Some anecdotally regard these species to be free of gyromitrin and safe to consume after thorough cooking. Others caution against eating any lorchels for fear that they may contain gyromitrin. Before our publication, no systematic study had been conducted to evaluate the distribution of gyromitrin in lorchels or the lorchel family broadly (Discinaceae).

​For more information on the chemistry of gyromitrin and a review of the relevant literature, please see the introduction in our paper, a PDF of which is available for free here.

Approach

We developed a new gyromitrin test. Our initial analyses were entirely qualitative (whether gyromitrin was present or absent), but later we developed a “standard curve” for quantitative analysis. Most samples in our paper were evaluated just for presence or absence of gyromitrin, but some were quantified. We sampled over 60 specimens (both mushrooms and mycelial cultures) from across Discinaceae, which besides Gyromitra includes truffles in the genus Hydnotrya and cup-shaped fungi in the genus Discina. Most samples came from North America. This study was largely conducted during the first two years of the Covid pandemic and our access to specimens from other parts of the world and funding was limited.

Three important caveats need to be mentioned:

1. We went for taxonomic breadth rather than depth since this paper is the foundation for evolutionary studies. These taxa of interst only had one or two specimens tested: Gyromitra americanigigas (1), Gyromitra brunnea (2), Gyromitra caroliniana (1), Gyromitra korfii (1), and Gyromitra montana (1). Gyromitra americanigigas was recently described from Northeastern North America and is morphologically indistinguishable from Gyromitra korfii and Gyromitra montana (Miller et al. 2022). No doubt it is misidentified as G. korfii and consumed as well.
2. Our test’s detection threshold for gyromitrin is 2 mg/kg dried fungal tissue. Specimens with less gyromitrin than this would show up as negative with our test. 
3. Some data presented below are from tests conducted after our study was published.

Results

Gyromitrin was readily detected (around 100-3,000 mg/kg dried tissue) in all tested specimens of the Gyromitra esculenta group, which consists of the following species:

• Gyromitra antarctica – South American species
• Gyromitra esculenta – European species
• Gyromitra splendida – primary species in Western North America, also present in Eastern North America and Europe
• Gyromitra venenata – primary species in Eastern North America, also present in Western North America; also present in Europe and Asia although its relative abundance compared to other species is unknown

Surprisingly, gyromitrin could be detected in very old mushrooms, including a specimen of Gyromitra venenata from the 1800s. 

Gyromitrin was also found in all tested specimens of a yellow cup fungus called Gyromitra leucoxantha, as well as a closely related, undescribed species from the Pacific Northwest (around 50-100 mg/kg dried tissue).

Gyromitrin was not detected in any other group.

​According to our phylogenetic tree, the distribution of gyromitrin could be a product of horizontal gene transfer.

Discussion

Specimens that tested negative in our study might actually contain gyromitrin at low levels. A European study from 1980 tested three specimens of Gyromitra gigas (closely related to G. americanigigas, G. korfii, and G. montana) and found gyromitrin at concentrations of 1.0 and 14.7 mg/kg dried tissue in two specimens (for comparison, our threshold is 2 mg/kg); the third had undetectable levels at their threshold of 0.5 mg/kg, if it was present at all (Viernstein et al. 1980). A clinical toxicology conference abstract reported that Gyromitra caroliniana contained “minute” amounts of gyromitrin, but the data were never published and cannot be evaluted (Liang et al. 1998).

​As the Gyromitra gigas data show, intraspecific variation in secondary metabolite production is a known phenomenon, meaning even if gyromitrin was absent from one specimen of a given species it could be present in another of that same species. 

Regarding the edibility of lorchels:

• The first thing to keep in mind is that gyromitrin is dangerous. Yes, methods exist to eat gyromitrin-containing lorchels without getting acutely sick, as is common in Scandinavia. If you decide to eat gyromitrin-containing lorchels you must be very careful. Personally, I'm not going to attempt to eat any Gyromitra esculenta group mushroom. 
• In my opinion, the best evidence for the edibilty of species like Gyromitra americanigigas, Gyromitra brunnea, Gyromitra caroliniana, Gyromitra korfii, and Gyromitra montana is the number of people who consume them without getting sick. They are presumably cooking them thoroughly and this is highly recommended for a safer (and tastier!) meal. There is no evidence of extraordinary poisoning from these mushrooms (most edible mushrooms, from chicken of the woods to morels to shiitake, have some reports of people getting sick due to misidentification, putrescent mushrooms, allergic responses, or perhaps unknown secondary metabolites). 
• For these five widely consumed species, we cannot definitively say that they do not produce gyromitrin, but rather there is no (strong) evidence that they produce gyromitrin (but see Liang et al. 1998). Given that Gyromitra gigas produces gyromitrin, I would bet that other Gyromitra gigas group species produce gyromitrin at low levels. We are going to test more specimens with heightened sensitivity.  
• The question that a prospective lorchel consumer must ask themself is, therefore, are they comfortable consuming species that might contain small amounts of gyromitrin? An answer either way is OK! Some things to consider: As a volatile substance, gyromitrin can be cooked away. Is it ever completely cooked away? Probably not. As a carcinogen and genotoxic substance, how much gyromitrin is too much gyromitrin? We don't know. Some studies suggest gyromitrin poisoning could be a factor in the development of neurodegenerative diseases (Lagrange et al. 2021). I expect as long as you don't get a large dose of gyromitrin you will be OK (I mean, not everyone in Finland who's eating well cooked Gyromitra esculenta group mushrooms has neurodegenerative disease?). But this is emerging research and is difficult to study. For the five species mentioned above that likely contain little to no gyromitrin, they might just deserve a California Proposition 65 carcinogen warning, a label that everything seems to have and nobody seems to care much about. 
• You must always positively identify the mushrooms you are consuming. "Gyromitra brunnea" is poisonous if you are actually eating Gyromitra venenata that you misidentified and have not prepared properly.
• I guess the usual disclamers should be said – be safe, these thoughts are my opinions and I'm not responsible for your decisions, and I wish you well. 

References

Dirks, A. C., Mohamed, O. G., Schultz, P. J., Miller, A. N., Tripathi, A., & James, T. Y. (2023). Not all bad: Gyromitrin has a limited distribution in the false morels as determined by a new ultra high-performance liquid chromatography method. Mycologia, 115(1), 1–15. 

Lagrange, E., Vernoux, J. P. P., Reis, J., Palmer, V., Camu, W., & Spencer, P. S. S. (2021). An amyotrophic lateral sclerosis hot spot in the French Alps associated with genotoxic fungi. Journal of the Neurological Sciences, 427(June), 1–8.

Liang, Y.-H., Eisenga, B. H., Trestrail, J. T. I., & Kuslikis, B. (1998). Gyromitra mushroom species and their monomethylhydrazine content. Platform Session 1: Part 2, Journal of Toxicology: Clinical Toxicology, 36(5), 527. 

Miller, A. N., Dirks, A. C., Filippova, N., Popov, E., & Methven, A. S. (2022). Studies in Gyromitra II: Cryptic speciation in the Gyromitra gigas species complex; rediscovery of G. ussuriensis and G. americanigigas sp. nov. Mycological Progress, 21(81), 1–13.

Viernstein, H., Jurenitsch, J., & Kubelka, W. (1980). Vergleich des giftgehaltes der lorchelarten Gyromitra gigas, Gyromitra fastigiata und Gyromitra esculenta. Ernahrung/Nutrition, 4(9), 392–395.