Understanding the electron pathway fluidity of Synechocystis in biophotovoltaics.

Biophotovoltaics offers a promising low-carbon footprint approach to utilize solar energy. It aims to couple natural oxygenic photosynthetic electrons to an external electron sink. This lays the foundation for a potentially high light-to-energy efficiency of the Biophotovoltaic process. However, there are still uncertainties around demonstrating the direct coupling of electron fluxes between photosystems and the external electrode. The dynamic cellular electron transfer network linked to physiological and environmental parameters poses a particular challenge here. In this work, the active cellular electron transfer network was modulated by tuning the cultivating conditions of Synechocystis and the operating conditions in Biophotovoltaics. The current output during darkness was found to be determined by the intracellular glycogen levels. Minimizing the intracellular glycogen pools also eliminated the dark-current output. Moreover, our results provide strong evidence that water splitting in photosystem II is the electron source enabling photocurrent, bypassing the microbe's metabolism. Eliminating the storage carbon as possible source of electrons did not reduce the specific photocurrent output, indicating an efficient coupling of photosynthetic electron flux to the anode. Furthermore, inhibiting respiration on the one hand increased the photocurrent and on the other hand showed a negative effect on the dark-current output. This suggested a switchable role of the respiratory electron transfer chain in the extracellular electron transfer pathway. Overall, we conclude that Synechocystis dynamically switches electron sources and utilizes different extracellular transfer pathways for the current output toward the external electron sink, depending on the physiological and environmental conditions.