Plants collect light for photosynthesis using light-harvesting complexes (LHCs)-an array of chlorophyll proteins that are able to reversibly switch from harvesting to energy-dissipation mode to prevent damage of the photosynthetic apparatus. LHC antennae as well as other members of the LHC superfamily evolved from cyanobacterial ancestors called high light-inducible proteins (Hlips). Here, we characterized a purified Hlip family member HliD isolated from the cyanobacterium Synechocystis sp. PCC 6803. We found that the HliD binds chlorophyll-a (Chl-a) and β-carotene and exhibits an energy-dissipative conformation. Using femtosecond spectroscopy, we demonstrated that the energy dissipation is achieved via direct energy transfer from a Chl-a Qy state to the β-carotene S1 state. We did not detect any cation of β-carotene that would accompany Chl-a quenching. These results provide proof of principle that this quenching mechanism operates in the LHC superfamily and also shed light on the photoprotective role of Hlips and the evolution of LHC antennae.

Background: PSII is a protein complex that captures sunlight to drive water oxidation. Results: Cyanidioschyzon merolae PSII is protected by reversible reaction center-based non-photochemical quenching. Conclusion: C. merolae PSII employs reaction center non-photochemical quenching as the main photoprotective mechanism. Significance: We provide the first direct evidence of the PSII reaction center as the primary locus of non-photochemical quenching in the extremophilic red algae.