Proton motive force dissipation drives flavodiiron proteins to the thylakoid membrane for ferredoxin-powered O2photoreduction

Abstract

AbstractFlavodiiron proteins (FDPs) catalyse light-dependent reduction of oxygen to water in photosynthetic organisms such as cyanobacteria, creating a protective electron sink that alleviates electron pressure on the photosynthetic apparatus. However, the electron donor to FDPs and the molecular mechanism regulating FDP activity have remained elusive. To address these questions, we employed spectroscopic and gas flux analysis of photosynthetic electron transport, bimolecular fluorescence complementation assays forin vivoprotein-protein interactions in the model cyanobacteriumSynechocystissp. PCC 6803, as well asin silicosurface charge modelling. We confirmed Ferredoxin-1 as the main electron donor to FDP heterooligomers and revealed that association of FDP heterooligomers with thylakoid membranes is promoted by dissipation of trans-thylakoid proton motive force. We propose a self-feedback mechanism to dynamically control FDP activity. Our findings elucidate the regulatory mechanisms of photosynthesis and have implications for rationally directing electron flux toward desired reactions in photosynthesis-based biotechnological applications.