Extracellular electron transfer through visible light induced excited-state outer membrane C-type cytochromes of Geobacter sulfurreducens

Dissimilatory metal-reducing bacteria (DMRB) have a variety of c-type cytochromes (OM c-cyts) intercalated in their outer membrane, and this structure serves as the physiological basis for DMRB to carry out the extracellular electron transfer processes. Using Geobacter sulfurreducens as a model DMRB, we demonstrated that visible-light illumination could alter the electronic state of OM c-cyts from the ground state to the excited state in vivo. The existence of excited-state OM c-cyts in vivo was confirmed by spectroscopy. More importantly, excited-state OM c-cyts had a more negative potential compared to their ground-state counterparts, conferring DMRB with an extra pathway to transfer electrons to semi-conductive electron acceptors. To demonstrate this, using a TiO₂-coated electrode as an electron acceptor, we showed that G. sulfurreducens could directly utilise the conduction band of TiO₂ as an electron acceptor under visible-light illumination (λ > 420 nm) without causing TiO₂ charge separation. When G. sulfurreducens was subject to visible-light illumination, the rate of extracellular electron transfer (EET) to TiO₂ accelerated by over 8-fold compared to that observed under dark conditions. Results of additional electrochemical tests provided complementary evidence to support that G. sulfurreducens utilised excited-state OM c-cyts to enhance EET to TiO₂.