Energetic decoupling of phycobilisomes from photosystem II involved in nonphotochemical quenching in red algae

To mitigate photodamage under fluctuating light conditions, photosynthetic organisms respond by regulating light energy absorbed by light-harvesting complexes and used for photochemistry. Nonphotochemical quenching acts as a frontline response to prevent excitation energy from reaching the photochemical reaction center of photosystem II. The mechanisms underlying nonphotochemical quenching in red algae, which display unique combination of light-harvesting transmembrane antenna proteins and membrane-attached phycobilisomes, appear to be different from those in cyanobacteria, green algae, and plants. Several single-process models have been proposed for red algal nonphotochemical quenching, yet the possibility of more than one process being involved in nonphotochemical quenching awaits further investigation. To assess multiple nonphotochemical quenching processes in the extremophilic red alga Cyanidioschyzon merolae, fluorescence analyses with light preferentially absorbed by phycobilisomes or photosystems were utilized. Energetic decoupling of phycobilisomes from photosystem II and intrinsic photosystem II quenching were identified as two dominant processes involved in nonphotochemical quenching and distinguished by their kinetics. Whereas the degrees of energetic decoupling remained similar after its induction, the degrees of intrinsic photosystem II quenching varied depending on the illumination period and intensity. The respective effects of protein crosslinkers, osmolytes, ionophores, and photosynthetic inhibitors on the kinetics of nonphotochemical quenching suggested that the energetic decoupling involved conformational changes associated with the connection between the PBS and PSII. Furthermore, the surface charge on the thylakoid membrane played a significant role in the modulation of red algal nonphotochemical quenching. One-sentence summaryEnergetic decoupling of phycobilisomes from photosystem II and intrinsic photosystem II quenching were involved in nonphotochemical quenching of the extremophilic red alga Cyanidioschyzon merolae.