Pyrite fuels electron fluxes to accelerate hydrocarbon removal in coastal wetland soil.

Natural sulfide minerals drive subsurface electron flow, but their role in hydrocarbon turnover is poorly understood. Here, we investigated whether pyrite (FeS2) can sustain electron transfer and accelerate petroleum hydrocarbon degradation in coastal wetland soils using a microbial electrochemical system (MES). High-dose pyrite amendment markedly enhanced long-term voltage output and increased cumulative charge by 34% over 120 days, indicating persistent subsurface electron release. Since pyrite improved soil conductivity and stimulated extracellular electron transfer, as reflected by elevated cytochrome c, extracellular polymeric substances production, and electroactive protein-like components. These electron transfer processes nearly doubled total petroleum hydrocarbon removal and promoted dissolved organic matter transformation from recalcitrant lignin-like compounds toward more bioavailable lipid- and protein-like components. Meanwhile, pyrite oxidation intensified Fe2 +/Fe3+ cycling, secondary iron mineral formation, and coupled carbon-iron-sulfur transformations. Metagenomic analysis further revealed enrichment of hydrocarbon degraders, electroactive microorganisms, sulfate reducers, and methanogens, together with upregulation of genes involved in carbon metabolism, nitrogen cycling, iron-sulfur transformation, conductive pili assembly, and ubiquinone biosynthesis. These findings identify pyrite as a geological energy node that fuels persistent subsurface electron fluxes to enhance hydrocarbon removal in coastal wetland soils, highlighting the potential of activating natural iron-sulfur minerals for in situ bioremediation in anoxic coastal zones.