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Unprecedented Mushroom Polyketide Synthases Produce the Universal Anthraquinone Precursor

Summary

Scientists discovered that mushrooms in the Cortinarius genus use unique enzymes called polyketide synthases to produce chemical building blocks that become anthraquinone compounds. These mushroom enzymes work differently from similar enzymes found in molds and plants, showing that nature independently invented multiple ways to make the same important molecules. This finding reveals how different organisms evolved similar chemical-making abilities through completely different evolutionary paths, and suggests this principle applies to many other mushroom species as well.

Background

Anthraquinones and pre-anthraquinones are bioactive natural products widely distributed across plants, fungi, bacteria, and invertebrates. The mushroom genus Cortinarius (webcaps) produces atrochrysone-derived pigments, but the genomic basis for their biosynthesis remained unknown. Previous research identified atrochrysone carboxylic acid synthases in molds and plants but not in mushrooms.

Objective

To identify and characterize the polyketide synthases responsible for atrochrysone carboxylic acid biosynthesis in the mushroom Cortinarius odorifer. To establish whether mushrooms use the same or different enzymatic pathways as ascomycete fungi and other organisms for anthraquinone precursor synthesis.

Results

CoPKS1 and CoPKS4 demonstrated atrochrysone carboxylic acid synthase activity, producing atrochrysone as the primary product. CoPKS4 uniquely catalyzed both heptaketide synthesis (6-hydroxymusizin) and octaketide synthesis. In vitro assays confirmed that CoPKS4 alone was sufficient for product formation without auxiliary thioesterase enzymes. Both CoPKS1 and CoPKS4 produced mixtures of enantiomers (3R and 3S configurations) in different ratios.

Conclusion

A novel class of SAT-domainless non-reducing polyketide synthases in mushrooms produces anthraquinone precursors, representing an independent evolutionary solution distinct from ascomycete enzymes. This discovery demonstrates convergent evolution of biosynthetic capacity across multiple kingdoms of life. The findings suggest a fundamental principle of fungal natural product chemistry applicable to numerous mushroom species.
  • Published in:Angewandte Chemie International Edition,
  • Study Type:Basic Research, Biochemical Characterization,
  • Source: PMID: 35218274, DOI: 10.1002/anie.202116142
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