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.

The direct coupling of the photosystem with the external anode is the theoretical basis of the BPV concept, for its capacity to explores the full potential of the oxygenic photosystem for energy production. However, there are still uncertainties in demonstrating such coupling, with conflicted results being reported in the past decade. In this work [1], we provide solid experimental basis to demonstrate that a BPV can extract electrons directly from the photosystem. We distinguished the cellular electron fluxes originating from water splitting in photosystem or those from degradation of the storage carbon via carbon metabolism, by tuning the cultivating conditions of the cyanobacteria and the operating conditions in BPV. Comparative analysis demonstrated that the current output during darkness was determined by the intracellular glycogen levels, and the current output during illumination could directly originate from the photosystems. The EET mechanism was demonstrated to be dynamic up to the environmental conditions and physiological status of the cyanobacterial cells.

Following up to the molecular dynamics of the EET pathways, we applied a comprehensive analytic approach to monitor the photosynthetic electron flows in Synechocystis sp. PCC 6803 cultivated in a ferricyanide-mediated BPV system [2]. 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. Knocking out the flv1/3 protein resulted in over 270% increase of the mediator reduction rate (i.e. the EET rate).