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

Abstract

Cable bacteria are filamentous sulphide-oxidisers performing long-distance electron transfer in redox-stratified sediments by transporting electrons over centimetre-scale distances to reduce oxygen. Here, we show that the freshwater cable bacterium Electronema aureum GS can respire insoluble electron acceptors under anoxic conditions via a versatile extracellular electron transfer (EET) system, supporting growth rates comparable to those under aerobic conditions. Using electrochemical and molecular biology analyses, we demonstrate that E. aureum GS engages in both direct and mediated electron transfer 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. Moreover, the redox shuttle riboflavin accumulated extracellularly and enhanced current production in bioelectrochemical systems, indicating a role for soluble mediators in cable bacteria. Together, these findings reveal a previously unrecognised respiratory flexibility in E. aureum GS and highlight EET as a key alternative strategy for energy conservation in fluctuating redox environments.