Hemin-binding DNA structures on the surface of bacteria promote extracellular electron transfer

Abstract

Recent research has shown that bacteria in anoxic layers ofPseudomonas aeruginosabiofilms can respire by transferring electrons to oxygen via extracellular DNA (eDNA) and DNA- binding redox mediators that are unique to this species1. In this study, we propose a similar but generic mechanism by which bacteria can transfer electrons via DNA in biofilms, using hemin as a redox-mediator and hemin-binding G-quadruplex (G4) DNA structures in the extracellular matrix.UsingStaphylococcus epidermidisas a model organism, voltammetry showed that eDNA and hemin were needed for extracellular electron transfer (EET). Surface-associated G4-DNA formed a complex with hemin, which transferred electrons from the bacteria to an electrode under anoxic conditions. Addition of G4-DNA and hemin to growing biofilms promoted EET which was stable for days. G4-DNA/hemin is also a peroxidase-like DNAzyme, capable of transferring electrons from bacteria to H2O2.G4-DNA were only recently discovered to be abundant in the extracellular matrix of biofilms2,3. We now show that hemin turns these structures into conduits for EET. The study opens the door to new and generic mechanisms for bacterial energy conservation under oxygen- limiting conditions, and for tackling H2O2, a common host defense mechanism against bacterial infections.