Ostroumov Evgeny E, Götze Jan P, Reus Michael, Lambrev Petar H, Holzwarth Alfred R
Max-Planck-Institut für Chemische Energiekonversion, Stiftstrasse 34-36, 45470, Mülheim a. d. Ruhr, Germany.
Quantum Matter Institute, University of British Columbia, 2355 East Mall, Vancouver, V6T 1Z1, Canada.
Photosynth Res. 2020 May;144(2):171-193. doi: 10.1007/s11120-020-00745-8. Epub 2020 Apr 20.
Light-harvesting complex II (LHCII) is the major antenna complex in higher plants and green algae. It has been suggested that a major part of the excited state energy dissipation in the so-called "non-photochemical quenching" (NPQ) is located in this antenna complex. We have performed an ultrafast kinetics study of the low-energy fluorescent states related to quenching in LHCII in both aggregated and the crystalline form. In both sample types the chlorophyll (Chl) excited states of LHCII are strongly quenched in a similar fashion. Quenching is accompanied by the appearance of new far-red (FR) fluorescence bands from energetically low-lying Chl excited states. The kinetics of quenching, its temperature dependence down to 4 K, and the properties of the FR-emitting states are very similar both in LHCII aggregates and in the crystal. No such FR-emitting states are found in unquenched trimeric LHCII. We conclude that these states represent weakly emitting Chl-Chl charge-transfer (CT) states, whose formation is part of the quenching process. Quantum chemical calculations of the lowest energy exciton and CT states, explicitly including the coupling to the specific protein environment, provide detailed insight into the chemical nature of the CT states and the mechanism of CT quenching. The experimental data combined with the results of the calculations strongly suggest that the quenching mechanism consists of a sequence of two proton-coupled electron transfer steps involving the three quenching center Chls 610/611/612. The FR-emitting CT states are reaction intermediates in this sequence. The polarity-controlled internal reprotonation of the E175/K179 aa pair is suggested as the switch controlling quenching. A unified model is proposed that is able to explain all known conditions of quenching or non-quenching of LHCII, depending on the environment without invoking any major conformational changes of the protein.
捕光复合物II（LHCII）是高等植物和绿藻中的主要天线复合物。有人提出，在所谓的“非光化学猝灭”（NPQ）中，激发态能量耗散的主要部分位于该天线复合物中。我们对聚集态和结晶态的LHCII中与猝灭相关的低能荧光态进行了超快动力学研究。在这两种样品类型中，LHCII的叶绿素（Chl）激发态都以类似的方式强烈猝灭。猝灭伴随着来自能量较低的Chl激发态的新的远红（FR）荧光带的出现。LHCII聚集体和晶体中猝灭的动力学、其低至4 K的温度依赖性以及FR发射态的性质非常相似。在未猝灭的三聚体LHCII中未发现此类FR发射态。我们得出结论，这些态代表弱发射的Chl-Chl电荷转移（CT）态，其形成是猝灭过程的一部分。对最低能量激子和CT态进行量子化学计算，明确包括与特定蛋白质环境的耦合，能够深入了解CT态的化学性质和CT猝灭机制。实验数据与计算结果相结合，有力地表明猝灭机制由涉及三个猝灭中心叶绿素610/611/612的两个质子耦合电子转移步骤组成。FR发射CT态是该序列中的反应中间体。E175/K179氨基酸对的极性控制内部质子化被认为是控制猝灭的开关。我们提出了一个统一模型，该模型能够解释LHCII猝灭或非猝灭的所有已知条件，这取决于环境，而无需调用蛋白质的任何重大构象变化。
