Desulfurella amilsii turns passivating sulfur into a self-regenerating S⁰/H₂S shuttle in a thermophilic bioanode

Polyextremophilic microorganisms offer a promising route to overcoming the biofilm acidification and cooling costs that limit microbial electrolysis cells (MECs), yet their use is frequently hindered by electrode passivation in sulfur-rich environments. Here we investigate whether the thermophilic, acid-tolerant bacterium Desulfurella amilsii TR1ᵀ can sustain anodic current through a sulfur-mediated mechanism. We report the first description of soluble iron reduction within the class Desulfurellia; however, physiological and electrochemical analyses revealed no evidence of a significant direct electron transfer (DET) contribution under our conditions. Instead, current generation relied on a functional S⁰/H₂S redox shuttle. By operating the poised bioanode under sulfur-depleted conditions, the system shifted from a low-efficiency regime to a balanced state in which the coulombic efficiency increased from <5% to >42%. These results demonstrate that the typically passivating sulfur layer can be exploited as a self-regenerating, solid-phase mediator, enabling sustained energy recovery at low anode potential (+0.1 to +0.5 V vs SHE) without requiring direct electrode respiration. This work therefore establishes the anodic basis for a future sulfur-mediated MEC, while hydrogen production at a dedicated cathode remains to be demonstrated.