Acclimation of Photosynthesis to the Environment 1 acts as a copper-binding superoxide detoxification enzyme

Plant acclimation is a growing scientific concept, at molecular, cellular and global scales. All photosynthetic organisms that created an oxic atmosphere on earth possess a gene of unknown function “Acclimation of Photosynthesis to the Environment 1”. Here we show that APE1 encodes a thylakoid-bound protein with a unique motif that binds copper and detoxifies the superoxide anion radical, O2•−. Maturation of the recombinant APE1 protein from Chlamydomonas reinhardtii requires formation of cysteine disulfide bonds after copper binding or via a high affinity interaction with a copper chaperone (Plastid Copper Chaperone 1) that boosts its scavenging capacity for O2•−. APE1 co-occurs in evolution with Photosystem II oxygen evolving proteins and it is the archaic O2•− detoxifying enzyme for acclimating photosynthesis to an oxygenic environment. APE1 co-evolved with Photosystem II as an ancestral enzyme that contributed to the Great Oxidation Event. This thylakoid-bound copper protein detoxifies O2•⁻, playing an essential role in photosynthetic acclimation to high light in oxic environments.