Activated OCP unlocks nonphotochemical quenching in cyanobacteria.

Most aerobic photosynthetic organisms have enough light-harvesting capacity so that on bright sunny days their photosynthesis is saturated for the major part of the day (1, 2). Early on in such sunny days the capacity of the reaction centers to process the absorbed solar energy is exceeded. The excess absorbed photons are potentially very dangerous. For example, if the chlorophyll-excited singlet states created in the antenna complexes cannot be used productively by the reaction centers, then these singlet states can potentially last long enough to undergo intersystem crossing to produce triplets. Excited chlorophyll triplet states can interact with molecular oxygen to produce very dangerous products, such as singlet oxygen (3). Singlet oxygen is an extremely powerful oxidizing molecule that can irreversibly damage lipids and, indeed, most major biological polymers. Cells exposed to singlet oxygen are rapidly killed (4). Oxygenic phototrophs have evolved a process, called nonphotochemical quenching (NPQ), to mitigate this problem of overexcitation (5). These phototrophs are able to control the efficiency of their light-harvesting systems. Under nonsaturating incident light intensities, the antenna complexes work as efficient light-harvesters, transferring absorbed solar energy effectively to the reaction centers. As incident light intensities become saturating, the antenna complexes switch to a quenched state, where the lifetime of their excited singlet states are strongly reduced and the efficiency of energy transfer to the reaction centers is much lower. The excess absorbed light-energy is effectively detoxified and converted harmlessly into heat. The process of NPQ has been extensively studied in plants and algae, where the major light-harvesting complexes are integral membrane chlorophyll-containing pigment-protein complexes (6). Cyanobacteria also show NPQ, but their major light-harvesting proteins are the water-soluble phycobiliproteins, where the light absorbing pigments are bilins (linear tetrapyroles) rather than chlorophylls (7). So how does NPQ work in this very different type of light-harvesting system? The answer involves a protein called the orange carotenoid protein (OCP) (8). Under nonsaturating incident light intensities, OCP remains orange and the phycobilisome functions as an efficient antenna system. When incident light becomes saturating, the excess light switches OCP into its active red form, called OCP. OCP interacts with the allophycocyanin molecules at the base of the phycobilisome to strongly accelerate the decay of the excited singlet states of the allophycobilin’s bilin pigments, thereby shutting down the efficiency of energy transfer from the phycobilisome to the photosynthetic reaction centers in the membrane (Fig. 1B) (6). It is as if OCP can close a “tap” at the end of the light-harvesting funnel to reduce the flow of energy through the funnel to the reaction centers in the photosynthetic membrane. The important question addressed in the paper by Gupta et al. (9) is: What are the structural changes occurring in OCP that underlie this form of NPQ? Previously, the groups of Kerfeld and Kirilovsky have collaborated to determine the X-ray crystal structures of both OCP (10) and OCP (11). However, they could only determine the structure of part of OCP because the complete protein, in this form, has up until now been resistant to attempts to crystallize it. PSII PSII