Crystal structure and functional peculiarities of a primordial Orange Carotenoid Protein (OCPX)

Abstract

The two-domain photoactive Orange Carotenoid Protein (OCP) confers photoprotection in cyanobacteria and presumably stems from domain fusion. Yet, the primitive thylakoid-less cyanobacteria Gloeobacter encodes a complete OCP. Its photosynthesis regulation lacks the so-called Fluorescence Recovery Protein (FRP), which in Synechocystis inhibits OCP-mediated phycobilisome fluorescence quenching, and Gloeobacter OCP belongs to the recently defined, heterogeneous clade OCPX (GlOCPX), the least characterized compared to OCP2 and especially OCP1 clades. Here we describe the first crystal structure of OCPX and provide its detailed structural and functional comparison with OCP1 from Synechocystis. Monomeric GlOCPX quenches Synechocystis phycobilisomes but displays drastically accelerated, less temperature-dependent recovery after photoactivation, evades regulation by FRP from other species and reveals numerous structural features reflecting its functional peculiarities. Our detailed description of a primordial OCPX sheds light on the evolution of the OCP-dependent photoprotection mechanism, rationalizing subdivision of the OCPX clade into subclades.