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Identification of two metallothioneins in Agaricus crocodilinus reveals gene duplication and domain expansion, a pattern conserved across fungal species

Summary

A common edible mushroom called A. crocodilinus can accumulate dangerous levels of cadmium from soil without being harmed. Scientists discovered this mushroom produces two different proteins called metallothioneins that work together to safely trap and store the toxic cadmium. One protein handles constant, everyday cadmium storage in the mushroom fruiting body, while the other activates quickly when the roots encounter sudden heavy metal stress. This same protective strategy appears in other mushroom species, showing it’s an important evolutionary adaptation.

Background

Agaricus crocodilinus, an edible saprotrophic mushroom, accumulates exceptionally high cadmium concentrations in unpolluted environments, reaching up to 249 mg Cd/kg dry tissue weight. This study investigates whether specialized metallothioneins (MTs), cysteine-rich proteins that bind heavy metal ions, contribute to cadmium detoxification and storage in this species.

Objective

To identify and characterize metallothionein genes in A. crocodilinus, determine their roles in metal sequestration, and investigate whether the gene duplication and domain expansion mechanisms identified are conserved across other fungal species.

Results

Two metallothionein genes were identified: AcMT1 (49 amino acids, 10 cysteines) and AcMT2 (32 amino acids, 7 cysteines). Mass spectrometry confirmed AcMT2 as the primary component of the 3.4 kDa cadmium-binding complex in sporocarps. AcMT2 is constitutively expressed, while AcMT1 is strongly induced under cadmium and copper stress. Genomic sequence analysis revealed that AcMT1 originated through internal domain duplication of an ancestral gene, a pattern conserved across other Agaricales and Boletales species.

Conclusion

A. crocodilinus employs two specialized metallothioneins with distinct roles: AcMT2 functions as a constitutive metal scavenger for baseline cadmium storage in mature sporocarps, while AcMT1 serves as an inducible rapid-response detoxifier activated under acute metal stress. Gene duplication and internal domain rearrangement represent conserved evolutionary mechanisms for metallothionein diversification in fungal species.
  • Published in:Biometals,
  • Study Type:Research Study,
  • Source: PMID: 40679729, DOI: 10.1007/s10534-025-00721-6
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