Mapping the Oxygens in the Oxygen-Evolving Complex of Photosystem II by Their Nucleophilicity Using Quantum Descriptors

The
oxygen-evolving complex (OEC) of Photosystem II catalyzes the
water-splitting reaction using solar energy. Thus, understanding the
reaction mechanism will inspire the design of biomimetic artificial
catalysts that convert solar energy to chemical energy. Conceptual
Density Functional Theory (CDFT) focuses on understanding the reactivity
of molecules and the atomic contribution to the overall nucleophilicity
and electrophilicity of the molecule using quantum descriptors. However,
this method has not been applied to the OEC before. Here, we use Fukui
functions and the dual descriptor to provide quantitative measures
of the nucleophilicity and electrophilicity of oxygens in the OEC
for different models in different S states. Our results show that
the μ-oxo bridges connected to terminal Mn4 are nucleophilic,
and those in the cube formed by Mn1, Mn2, and Mn3 are mostly electrophilic.
The dual descriptors of the bridging oxygens in the OEC showed a similar
reactivity to that of bridging oxygens in Mn model compounds. However,
the terminal water W1, which is bound to Mn4, showed very strong reactivity
in some of the S3 models. Thus, our calculations support
the model that proposes the formation of the O2 molecule
through nucleophilic attack by a terminal water.

光系统II（Photosystem II）的放氧复合体（oxygen-evolving complex，OEC）可利用太阳能催化水分解反应。因此，阐明其反应机制将为可将太阳能转化为化学能的仿生人工催化剂的设计提供理论借鉴。概念性密度泛函理论（Conceptual Density Functional Theory，CDFT）旨在通过量子描述符解析分子的反应活性，以及各原子对分子整体亲核性与亲电性的贡献，但此前该方法尚未被应用于放氧复合体的相关研究。本研究采用福井函数（Fukui functions）与双描述符（dual descriptor），针对不同S态下的多种模型，定量表征了放氧复合体中氧原子的亲核性与亲电性。研究结果表明，与末端Mn4相连的μ-氧桥表现出亲核性，而由Mn1、Mn2与Mn3构成的立方结构中的μ-氧桥则大多呈现亲电性。放氧复合体中桥连氧原子的双描述符特征，与锰模型化合物中的桥连氧原子反应活性相似。但绑定于Mn4的末端水分子W1，在部分S3模型中展现出极强的反应活性。因此，本研究的计算结果支持"氧气分子通过末端水分子的亲核进攻生成"这一反应模型。