Periplasmic FeS Electron Conduits: Tuning Electrocoupling and Respiratory Dehalogenation in a Synthetic Consortium

Electron delivery within and between bacterial cells is a central bottleneck in anaerobic biotransformation of electron acceptor-type substrates (EATS). Using hexabromocyclododecane (HBCD) as a model organohalogen, we developed a cysteine desulfhydrase (CSD)-associated periplasmic FeS biomineralization strategy in a defined synthetic consortium. CSD-associated FeS formation enabled rapid installation of FeS conduits in non-sulfate-reducing bacteria within ∼3 h, forming predominantly periplasmic conductive interfaces that lowered interfacial charge-transfer resistance and increased capacitive electron storage. Electrochemical analyses revealed coculture-specific electron-transfer behavior, increased electron-accepting capacity, and enhanced transport activity; cocultures outperformed monocultures, consistent with strengthened interspecies electron transfer. Detection of lower-brominated intermediates and bromide release supported dihaloelimination-dominated debromination, with Fe-matched cell-free FeS accounting for only 2.8% of the live-cell Br^- signal. Inhibitor profiling further suggested that FeS alters electron-transfer behavior from NADH/menaquinone-linked steps toward terminal reductive processes, consistent with relief of respiratory bottlenecks. Structure prediction and docking support a working model in which a QueG-like, cobalamin-dependent candidate terminal reductase may participate in HBCD reduction, while FeS conduits enhance local electron delivery, charge-transfer behavior, and whole-cell debromination. Overall, periplasmic FeS conduits provide a CSD-associated interfacial strategy to modulate electron flux in this defined coculture, highlighting a potentially transferable route for transforming emerging organohalogens and other EATS.