Bhattacharjee Sinjini, Gordiy Igor, Sirohiwal Abhishek, Pantazis Dimitrios A
Department of Molecular Theory and Spectroscopy, Max-Planck-Institut für Kohlenforschung, Mülheim an der Ruhr 45470, Germany.
Department of Inorganic and Physical Chemistry, Division of Chemical Sciences, Indian Institute of Science, Bangalore 560012, India.
Proc Natl Acad Sci U S A. 2025 May 20;122(20):e2417963122. doi: 10.1073/pnas.2417963122. Epub 2025 May 12.
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.
光系统II（PSII）是一种蛋白质色素复合体，它利用阳光催化水氧化和质体醌还原，启动有氧光合作用中的电子转移（ET）级联反应。D1和D2蛋白是PSII最重要的跨膜亚基，它们结合了参与原初电荷分离（CS）和ET的所有氧化还原活性成分。D1易受氧化光损伤，特别是在强光下，其保护部分涉及基因调控。蓝细菌D1由基因家族编码，该家族根据环境条件表达不同的异构体（PsbA1-3）。D1异构体的大多数差异靠近活性分支反应中心（RC）色素P、P、Chl和Pheo。在这里，我们将分子动力学模拟与对每个变体的膜结合PSII单体进行的多尺度量子力学/分子力学计算相结合，使用长程校正密度泛函理论比较RC色素的氧化还原和激发态性质。我们确定了导致不同色素和色素基团发生电致变色位移的特定氨基酸取代。我们的结果表明，Pheo受体是主要的调控靶点。Chl-Pheo对的氧化还原性质和ChlPheo电荷转移态的能量在三种异构体中受到明显调节：与标准PSII相比，PSII中的电荷分离受到抑制，而PSII中的电荷分离则得到促进。这些结果提供了一个微观描述，说明基因变异如何调节蛋白质静电并影响光合反应中心的初级过程。
