Interaction between the oxidative pentose phosphate pathway and chlororespiration sustains high-rate algal...

Photosynthetic microorganisms enable the conversion of sunlight into electricity via exoelectrogenesis - the export of electrons to the extracellular environment. However, current strategies to enhance this process often rely on nutrient deprivation, such as iron limitation, which inevitably compromises the photosynthetic apparatus and arrests cell growth. Here, we investigate the physiological basis of the inherently enhanced exoelectrogenesis in the green microalga Parachlorella kessleri MACC-38 - a strain that exhibits tenfold higher electric current production than the model alga Chlamydomonas reinhardtii without requiring stress treatments. We propose that upon exposure to ferricyanide as an extracellular electron sink, the oxidative pentose phosphate pathway (OPPP) is upregulated - specifically via glucose-6-phosphate dehydrogenase - to supply NADPH as the primary reducing power for exoelectrogenesis. Furthermore, we suggest that while the OPPP supports electron export, it simultaneously induces a transient over-reduction of the photosynthetic electron transport chain. Our data indicates that chlororespiration, mediated by the plastid terminal oxidase (PTOX), is essential to maintain redox homeostasis by re-oxidizing the plastoquinone pool, while sustaining exoelectrogenesis. These results may find application in the rational design of highly exoelectrogenic microorganisms with synthetic biology tools for sustainable, high-efficiency biophotovoltaic systems.