Factors Controlling the Redox Potential of ZnCe6 in an Engineered Bacterioferritin Photochemical ‘Reaction Centre’

Photosystem II (PSII) of photosynthesis has the unique ability to photochemically oxidize water. Recently an engineered bacterioferritin photochemical ‘reaction centre’ (BFR-RC) using a zinc chlorin pigment (ZnCe6) in place of its native heme has been shown to photo-oxidize bound manganese ions through a tyrosine residue, thus mimicking two of the key reactions on the electron donor side of PSII. To understand the mechanism of tyrosine oxidation in BFR-RCs, and explore the possibility of water oxidation in such a system we have built an atomic-level model of the BFR-RC using ONIOM methodology. We studied the influence of axial ligands and carboxyl groups on the oxidation potential of ZnCe6 using DFT theory, and finally calculated the shift of the redox potential of ZnCe6 in the BFR-RC protein using the multi-conformational molecular mechanics–Poisson-Boltzmann approach. According to our calculations, the redox potential for the first oxidation of ZnCe6 in the BRF-RC protein is only 0.57 V, too low to oxidize tyrosine. We suggest that the observed tyrosine oxidation in BRF-RC could be driven by the ZnCe6 di-cation. In order to increase the efficiency of tyrosine oxidation, and ultimately oxidize water, the first potential of ZnCe6 would have to attain a value in excess of 0.8 V. We discuss the possibilities for modifying the BFR-RC to achieve this goal.

光系统II（Photosystem II, PSII）是光合作用中唯一具备光化学氧化水能力的复合物。近期研究发现，一种经工程改造的细菌铁蛋白光化学“反应中心”（engineered bacterioferritin photochemical reaction centre, BFR-RC），以锌氯啉色素（zinc chlorin pigment, ZnCe6）替代其天然血红素，可通过酪氨酸残基光氧化结合态锰离子，从而模拟光系统II电子供体侧的两项关键反应。为阐明BFR-RC中酪氨酸氧化的机制，并探索此类体系实现水氧化的可能性，我们采用ONIOM方法构建了该反应中心的原子级模型。我们借助密度泛函理论（Density Functional Theory, DFT）研究了轴向配体与羧基基团对ZnCe6氧化还原电位的影响，并最终通过多构象分子力学-泊松-玻尔兹曼（multi-conformational molecular mechanics–Poisson-Boltzmann）方法计算了BFR-RC蛋白内ZnCe6的氧化还原电位偏移量。计算结果表明，BRF-RC蛋白中ZnCe6的首次氧化还原电位仅为0.57 V，不足以氧化酪氨酸。我们推测，观测到的BRF-RC内酪氨酸氧化过程可由ZnCe6双阳离子驱动。若要提升酪氨酸氧化效率并最终实现水氧化，ZnCe6的首次氧化还原电位需提升至0.8 V以上。最后我们讨论了改造BFR-RC以达成该目标的潜在可行路径。