Integrated multi-omics reveals mycelial spatial restructuring and coordinated metabolic reprogramming underlying fungal iron detoxification in Leucocalocybe mongolica

Abstract

Global soil contamination with heavy metals threatens food security and ecosystem health. This study investigates the potential of saprotrophic fungus Leucocalocybe mongolica (LY9) to immobilize and detoxify iron. Soil amendment with LY9 reduces iron bioavailability in a dose-dependent manner, with the 50% treatment decreasing soil iron by 28.3%. Spatial ionomic analysis shows the fungal mycelium forms a sequestration gradient, actively mobilizing soluble iron and depleting it by 26.9% in densely colonized zones. Under 25 mg/L Fe²⁺ stress, LY9 shows strong tolerance and accumulates iron in biomass, peaking at 41.23 mg/kg on day 15 (Fe15). Integrated multi-omics analyses at Fe15 uncover a refined adaptation strategy: coordinated upregulation of genes for iron-sulfur cluster biogenesis, antioxidant defense (e.g., glyoxalase I, GSTs, Mn-SOD), energy metabolism (ETC, TCA cycle), and cell wall fortification (hydrophobins, CAZymes). This transcriptional reprogramming is mirrored by the metabolome, with a massive >124-fold accumulation of glutathione and its precursor (γ-glutamylcysteine), plus a > 50-fold increase in NAD + /NADP+ and a > 200-fold increase in AMP, highlighting a coordinated metabolic shift toward antioxidant defense and energy production to combat iron-induced oxidative stress. Our findings show LY9 uses a multi-level strategy, from ecosystem engineering to molecular reprogramming, establishing it as a promising candidate for bioremediating iron-toxic soils.