Cu+ Contributes to the Orange Carotenoid Protein-Related Phycobilisome Fluorescence Quenching and Photoprotection in Cyanobacteria.

Photosynthesis starts with absorption of light energy by using light-harvesting antenna complexes (LHCs). Overexcitation of LHCs and subsequent photosystems, however, is damaging and can be lethal. The orange carotenoid protein (OCP) protects most cyanobacteria from photodamage by dissipating excessive excitation energy harvested by phycobilisomes (PBS, LHCs) as heat. OCP has two states: the orange, inactive OCP (OCPO) and the red, active OCP (OCPR), with the latter able to bind PBS at a ratio of 2:1 and execute photoprotection. Conversion of OCPO to OCPR is driven by blue light absorption. Previous work indicated that in the presence of Cu2+, photoactivation of OCP can result in it being locked in its red form OCPR. The molecular mechanism of such chemical conversion, however, remains unclear. Here, we demonstrated that Cu+ can convert OCPO to OCPR under anaerobic conditions independent of light illumination. Interestingly, in the presence of Cu2+ and ascorbic acid, a ubiquitous reductant in photosynthetic organisms, the conversion of OCPO to OCPR can also take place spontaneously in the dark, indicative of a locked OCPR-Cu+ complex. Furthermore, our functional and structural studies indicate that OCPR-Cu+ can interact with PBS and trigger PBS fluorescence quenching. We hypothesize that copper ion, a redox-active component, may synergistically play an important role in the regulation of nonphotochemical quenching in cyanobacteria under stress conditions.