Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system.

Abstract

Biophotovoltaics (BPV) represents an innovative biohybrid technology that couples electrochemistry with oxygenic photosynthetic microbes to harness solar energy and convert it into electricity. Central to BPV systems is the ability of microbes to perform extracellular electron transfer (EET), utilizing an anode as an external electron sink. This process simultaneously serves as an electron sink and enhances the efficiency of water photolysis compared to conventional electrochemical water splitting. However, optimizing BPV systems has been hindered by a limited understanding of EET pathways and their impacts on cellular physiology. Here we show photosynthetic electron flows in Synechocystis sp. PCC 6803 cultivated in a ferricyanide-mediated BPV system. By monitoring carbon fixation rates and photosynthetic oxygen exchange, we reveal that EET does not significantly affect cell growth, respiration, carbon fixation, or photosystem II efficiency. However, EET competes for electrons with the flavodiiron protein flv1/3, influencing Mehler-like reactions. Our findings suggest that the ferricyanide mediator facilitates photosynthetic electron extraction from ferredoxins downstream of photosystem I. Additionally, the mediator induces a more reduced plastoquinone pool, an effect independent of EET. At very high ferricyanide concentrations, the electron transport chain exhibits responses resembling the impact of trace cyanide. These insights provide a molecular-level understanding of EET pathways in Synechocystis within BPV systems, offering a foundation for the future refinement of BPV technologies.