The primary donor of far-red photosystem II: Chl_D1 or P_D2?

Far-red light (FRL) Photosystem II (PSII) isolated from Chroococcidiopsis thermalis is studied using parallel analyses of low-temperature absorption, circular dichroism (CD) and magnetic circular dichroism (MCD) spectroscopies in conjunction with fluorescence measurements. This extends earlier studies (Nurnberg et al 2018 Science 360 (2018) 1210-1213). We confirm that the chlorophyll absorbing at 726 nm is the primary electron donor. At 1.8 K efficient photochemistry occurs when exciting at 726 nm and shorter wavelengths; but not at wavelengths longer than 726 nm. The 726 nm absorption peak exhibits a 21 ± 4 cm^-1 electrochromic shift due to formation of the semiquinone anion, Q_A^-. Modelling indicates that no other FRL pigment is located among the 6 central reaction center chlorins: P_D1, P_D2 Chl_D1, Chl_D2, Pheo_D1 and Pheo_D2. Two of these chlorins, Chl_D1 and P_D2, are located at a distance and orientation relative to Q_A^- so as to account for the observed electrochromic shift. Previously, Chl_D1 was taken as the most likely candidate for the primary donor based on spectroscopy, sequence analysis and mechanistic arguments. Here, a more detailed comparison of the spectroscopic data with exciton modelling of the electrochromic pattern indicates that P_D2 is at least as likely as Chl_D1 to be responsible for the 726 nm absorption. The correspondence in sign and magnitude of the CD observed at 726 nm with that predicted from modelling favors P_D2 as the primary donor. The pros and cons of P_D2 vs Chl_D1 as the location of the FRL-primary donor are discussed.