Electrode-Triggered niche differentiation and endogenous electron cycling boost bioremediation of mixed aromatic contaminants in oligotrophic groundwater

Chlorinated and non-chlorinated aromatic contaminants frequently co-occur in groundwater, but their synergistic bioremediation is often hindered by conflicting redox requirements, microbial niche competition, and the need for external organic carbon sources. Here, we present an electro-stimulated bio-circulation well (ES-BCW) that couples electrode-mediated redox regulation with internal hydraulic recirculation, enabling the simultaneous continuous reductive dechlorination and oxidative aromatic degradation without exogenous organic carbon supplementation. Under continuous operation (120 d), the ES-BCW system achieved average removal rates of 53.2 µmol L⁻¹ d⁻¹ for 1,2,4-trichlorobenzene (1,2,4-TCB) and 169.5 µmol L⁻¹ d⁻¹ for toluene, respectively, demonstrating competitive performance for anaerobic co-treatment of mixed aromatic contaminants. Optimal weak electrical stimulation (1.2 V) with a controlled reflux (50%) promoted spatial niche differentiation between cathodic reductive and anodic oxidative zones. Microbial analysis revealed selective enrichment of dechlorinating (Dechloromonas and Sphingobium), toluene-degrading (Azoarcus and Thauera), and electroactive (Geobacter and Sulfurospirillum) genera. Integrated metagenomic and metabolomic analyses revealed coordinated enrichment of dechlorination (pcpB, pcpC) and toluene oxidation (bssABC, bbsG) genes, coupled with increased abundances of energy carriers and key electron transfer components (i.e. cytochromes). These shifts collectively supported enhanced electron flux redistribution, metabolic synergy, and sustained acetate cycling, establishing a self-amplifying loop of endogenous carbon reuse that enabled redox partitioning between cathodic reductive and anodic oxidative niches. The ES-BCW system offers an endogenous carbon-driven strategy for synergistic bioremediation of mixed aromatic contaminated oligotrophic groundwater.