Extracellular electron transfer in cable bacteria enables growth rates comparable to aerobic respiration

Cable bacteria are filamentous sulphide-oxidising bacteria that transport electrons through conductive periplasmic fibres over centimetre-scale distances in redox-stratified sediments to respire oxygen. Here, we show that the freshwater cable bacterium Electronema aureum GS employs a versatile extracellular electron transfer (EET) system to respire insoluble electron acceptors under anoxic conditions, achieving growth rates comparable to aerobic respiration. Electrochemical and molecular analyses reveal that E. aureum GS performs both direct and riboflavin-mediated EET to electrodes, including at +600 mV vs. Ag/AgCl, an unusually high redox potential typically not accessed by electroactive bacteria. Two distinct cell-surface redox components were identified, which are metal-dependent, pH-sensitive, and heat-labile, consistent with outer-membrane-localised cytochromes. The redox shuttle riboflavin accumulated in bioelectrochemical systems with E. aureum GS, supporting mediated EET. These findings reveal a respiratory flexibility in E. aureum GS and highlight the role of EET in energy conservation in dynamic redox environments.