Self-Damaging Aerobic Reduction of Graphene Oxide by Escherichia coli: Role of GO-Mediated Extracellular Superoxide Formation

Microbial reduction of graphene oxide (GO) under aerobic conditions is poorly understood despite its critical role in changing GO toxicity and environmental fate. Here we show that 20 mg/L GO interacts with the membrane-bound cytochrome c of E. coli in saline, shuttling electrons from the respiratory chain to extracellular molecular oxygen. This results in the formation of superoxide anions (O2•–), which in turn reduce GO in 30 min. The critical role of superoxide was demonstrated by impeding GO reduction upon addition of superoxide dismutase, or by carrying out experiments under strictly anaerobic conditions that preclude O2•– formation. Coating GO with bovine serum albumin also stopped GO reduction, which indicates the need for direct contact between GO and the cell membrane. Cell death was observed as a consequence of GO bioreduction. Apparently, electron shuttling by GO (via membrane contact) interrupts the respiratory chain and induces oxidative stress, as indicated by a 20% decrease in electron transport activity and an increase in intracellular reactive oxygen species. This novel antimicrobial mechanism could be relevant to assess GO stability and biocompatibility, and informs potential applications for microbial control.