Oxygen drives a rapid, reversible photoprotective switch in photosynthetic antennae

Abstract

Oxygen is the archetypal agent of photooxidative damage, and it is generally countered by removing its reactive products or by regulated, energy-costly responses. We show that in photosynthetic light-harvesting complexes, oxygen also drives a rapid, reversible photoprotective switch. Using a new bulk fluorescence method that separates reversible dark states from irreversible photobleaching, together with single-molecule spectroscopy, we find that illumination and oxygen generate a reversible, protein-stabilized charge-separated state comprising oxidized chlorophyll and superoxide. Access to this state increasingly outcompetes irreversible photodamage as excitation intensity falls to physiological levels and is strongly accelerated by ascorbic acid in native thylakoid membranes. These findings identify a constitutive oxygen-dependent photoprotective pathway and suggest that redox-state recovery can determine whether oxygen-associated chemistry protects or damages photoactive systems.