Evolution of the Structure and Function of the Cyanobacterial Orange Carotenoid Protein and its Quenching of the Cyanobacterial Light Harvesting Antenna

In contrast to those of plants, the photoprotective mechanisms of cyanobacteria have only recently begun to be characterized. One of the most prevalent, involving the Orange Carotenoid Protein (OCP), a photoreceptor, dissipates excess energy captured by the light harvesting antenna (phycobilisome or PBS). The OCP is a soluble, 34 kDa protein that binds a single carotenoid molecule. It is the only known photoactive protein that uses a carotenoid as its sole chromophore. The crystal structure of the OCP^O shows that the protein is comprised of two structural domains: a carotenoid-binding N-terminal domain (NTD), unique to cyanobacteria, and a C-terminal domain (CTD) with superficial structural similarity to BLUF and LOV domains. The carotenoid spans the two domains. The absorption of blue-green light causes the OCP to convert from a dark stable orange form, OCP^O, to a light-activated red form, OCP^R. Structurally the photoactivation is characterized by a 12Å shift in the position of the carotenoid and, as recently revealed by our Cryo-EM structure of the quenching complex between the OCP and the PBS, a 60Å/220 degree rotation of the CTD. The structure of the OCP^R -PBS complex also provides a high-resolution structural description showing how four 34kDa OCPs, each with a single carotenoid, are able to quench the 6.3MDa PBS with its 396 bilin pigments. In conjunction with analysis of genomic sequence data from ecophysiologically diverse cyanobacteria we find a variety of carotenoproteins that are single-domains homologs of the OCP. Collectively our observations suggest a model for the evolution of OCP-mediated photoprotection and provide a framework for co-opting elements of the OCP structurally and functionally for the development of optogenetic and artificial photosynthesis systems.