Equipped for success : genomes and metabolomes of the European Amanita muscaria are conserved in its novel South African range
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Wiley
Abstract
• Plants and soils have been moved around the world for centuries, but invasive mushrooms receive scant attention. The Amanita muscaria species complex was introduced to South Africa in the context of forestry, but its origins, ecology and recent evolution are unstudied.
• We sequenced the genomes of 24 Northern and Southern Hemisphere A. muscaria, built phylogenies and reconstructed its South African history. We identified the biosynthetic gene clusters (BGCs) encoding specialized metabolites (SMs). We subsequently extracted mushrooms' metabolites and used mass spectrometry data to group SMs into unique molecular families (MFs). We tested metabolites for bioactivity against diverse microbes and animals.
• We identify Europe as the origin of South African A. muscaria. A highly conserved group of BGCs is found in nearly all European and African genomes, and only 13 of 273 MFs are unique to South Africa. Metabolites extracted from all mushrooms kill nematodes, while microbes and flies appear unaffected.
• The nearly global distribution of the fly agaric results from multiple introductions of a single European clade to the Southern Hemisphere. Despite its long history in South Africa, the fungus has not lost any of its BGCs, suggesting a conservation of function(s) across multiple continents.
Description
DATA AVAILABILITY : All genomic data used in our study are either publicly available through NCBI (see the Materials and Methods section and Dataset S2) or were generated by the authors and are made public with our publication. Raw sequencing reads and genome assemblies are available through NCBI BioProject (accession no.: PRJNA1372216). The screening methods used to test bioactivities and raw results are provided in Supporting Information (Figs S11–S15). The Supporting Information also provides details on genome annotation (Methods S1), mitogenome analysis (Methods S1), split decomposition of the SNP dataset (Methods S1) and targeted genome mining for amatoxin-encoding genes (Methods S1). Supporting Datasets include a summary of genome summary statistics (Dataset S1), the gene markers used to generate Fig. 2 (Dataset S2) and the results of our kinship analysis (Dataset S3).
SUPPLEMENTARY MATERIAL 1 :
DATASET S1 Genome summary statistics.
DATASET S2 Full metadata for Amanita muscaria data retrieved from prior publications.
DATASET S3 Kinship analyses of the sequenced genomes.
SUPPLEMENTARY MATERIAL 2 :
FIG. S1 Dried tissue of each mushroom prior to chemical analyses.
FIG. S2 Determination of optimal cutoff to generate the PKS GCF predictions.
FIG. S3 Determination of optimal cutoff to generate the Terpene GCF predictions.
FIG. S4 Rooted phylogenies from the fully sequenced Amanita muscaria genomes.
FIG. S5 Tree compatibility comparisons between different species reconstruction methods.
FIG. S6 A cblaster analysis showing the presence and absence of genes in the ibotenic acid cluster in Amanita muscaria and outgroup genomes.
FIG. S7 Whole fungal kingdom phylogeny depicting the number of Reciprocal best-hit BLAST hits to genes in the ibotenic acid gene cluster.
FIG. S8 Quantity of putative muscimol in every sample.
FIG. S9 Comparison of polyketide synthases found in Amanita
Keywords
Global natural product social molecular networking analysis, Invasive ectomycorrhizal fungi, Invasive mushrooms, Secondary or specialized metabolites, Metabolism, South Africa (SA), Bioactivity, Biosynthetic gene clusters (BGCs), Fly agaric, Amanita muscaria
Sustainable Development Goals
SDG-15: Life on land
Citation
Nickles, G.R., Stokes, C.K., Narh, D.L. et al. 2026, 'Equipped for success: genomes and metabolomes of the European Amanita muscaria are conserved in its novel South African range', New Phytologist, vol. 250, no. 3, pp. 1863-1883. https://doi.org/10.1111/nph.71064.