Microscopic basis of reaction center modulation in PsbA variants of photosystem II.

Photosystem II (PSII) is a protein-pigment complex that utilizes sunlight to catalyze water oxidation and plastoquinone reduction, initiating the electron transfer (ET) cascade in oxygenic photosynthesis. The D1 and D2 proteins are the most important transmembrane subunits of PSII that bind all redox-active components involved in primary charge separation (CS) and ET. D1 is susceptible to oxidative photodamage, particularly under high light, and protection partly involves genetic regulation. Cyanobacterial D1 is encoded by the gene family that expresses distinct isoforms (PsbA1-3) depending on environmental conditions. Most differences in D1 isoforms are close to the active-branch reaction center (RC) pigments P, P, Chl, and Pheo. Here, we combine molecular dynamics simulations with multiscale quantum-mechanics/molecular-mechanics calculations on the membrane-bound PSII monomer of each variant to compare the redox and excited state properties of RC pigments using long-range-corrected density functional theory. We identify specific amino acid substitutions responsible for electrochromic shifts on distinct pigments and pigment groups. Our results indicate that the Pheo acceptor is the primary regulatory target. The redox properties of the Chl-Pheo pair and the energetics of ChlPheo charge-transfer states are distinctly modulated in the three isoforms: Compared to the standard , charge separation is inhibited in and facilitated in PSII. The results provide a microscopic description of how genetic variations modulate protein electrostatics and influence primary processes in photosynthetic reaction centers.