Department of Chemistry, Yale University, New Haven, CT 06520-8107.
Institute of High Performance Computing, Agency for Science, Technology and Research, Singapore 138632.
Proc Natl Acad Sci U S A. 2017 Jul 11;114(28):E5513-E5521. doi: 10.1073/pnas.1614857114. Epub 2017 Jun 26.
In photosynthetic organisms, protection against photooxidative stress due to singlet oxygen is provided by carotenoid molecules, which quench chlorophyll triplet species before they can sensitize singlet oxygen formation. In anoxygenic photosynthetic organisms, in which exposure to oxygen is low, chlorophyll-to-carotenoid triplet-triplet energy transfer (T-TET) is slow, in the tens of nanoseconds range, whereas it is ultrafast in the oxygen-rich chloroplasts of oxygen-evolving photosynthetic organisms. To better understand the structural features and resulting electronic coupling that leads to T-TET dynamics adapted to ambient oxygen activity, we have carried out experimental and theoretical studies of two isomeric carotenoporphyrin molecular dyads having different conformations and therefore different interchromophore electronic interactions. This pair of dyads reproduces the characteristics of fast and slow T-TET, including a resonance Raman-based spectroscopic marker of strong electronic coupling and fast T-TET that has been observed in photosynthesis. As identified by density functional theory (DFT) calculations, the spectroscopic marker associated with fast T-TET is due primarily to a geometrical perturbation of the carotenoid backbone in the triplet state induced by the interchromophore interaction. This is also the case for the natural systems, as demonstrated by the hybrid quantum mechanics/molecular mechanics (QM/MM) simulations of light-harvesting proteins from oxygenic (LHCII) and anoxygenic organisms (LH2). Both DFT and electron paramagnetic resonance (EPR) analyses further indicate that, upon T-TET, the triplet wave function is localized on the carotenoid in both dyads.
在光合作用生物体中，类胡萝卜素分子为防止单线态氧引起的光氧化应激提供了保护，它们在叶绿素三重态物质能够敏化单线态氧形成之前将其猝灭。在缺氧光合作用生物体中，由于氧气暴露水平低，叶绿素-类胡萝卜素三重态-三重态能量转移（T-TET）速度较慢，范围在数十纳秒内，而在富含氧气的产氧光合作用叶绿体中则超快。为了更好地理解导致适应环境氧气活性的 T-TET 动力学的结构特征和由此产生的电子耦合，我们对具有不同构象的两种异构类胡萝卜素卟啉分子二聚体进行了实验和理论研究，因此具有不同的发色团间电子相互作用。这对二聚体再现了快速和慢速 T-TET 的特征，包括在光合作用中观察到的强电子耦合和快速 T-TET 的基于共振拉曼的光谱标记。如密度泛函理论（DFT）计算所确定的，与快速 T-TET 相关的光谱标记主要归因于三重态中发色团间相互作用引起的类胡萝卜素骨架的几何扰动。这对于自然系统也是如此，正如来自含氧（LHCII）和缺氧生物（LH2）的光捕获蛋白的混合量子力学/分子力学（QM/MM）模拟所证明的那样。DFT 和电子顺磁共振（EPR）分析进一步表明，在 T-TET 后，两个二聚体中的三重态波函数都定域在类胡萝卜素上。
