Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer
Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer
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DOI：
10.1073/pnas.2018240118
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发表时间：
2021-03-16
影响因子：
11.1
通讯作者：
Engel, Gregory S.
中科院分区：
文献类型：
--
作者：
Higgins, Jacob S.;Lloyd, Lawson T.;Engel, Gregory S.
光合物种进化以保护其捕光器免受由细胞内氧化还原条件或环境条件驱动的光氧化损伤。来自绿色硫细菌的Fenna-Matthews-Olson（FMO）色素-蛋白质复合物表现出氧化还原依赖的猝灭行为，部分归因于两个内部半胱氨酸残基。在这里，我们证明了光合复合物利用振动混合的量子力学来激活氧化光保护机制的证据。我们使用二维电子光谱（2DES）捕捉能量转移动力学在野生型和半胱氨酸缺陷FMO突变蛋白在还原和氧化条件下。在还原条件下，我们发现相等的能量转移通过激子4-1和4-2-1途径，因为激子4-1的能隙是振动耦合的细菌叶绿素-a振动模式。然而，在氧化条件下，激子4-1能隙的共振与振动模式失谐，导致激子优先通过间接4-2-1途径转向，以增加激子淬灭的可能性。我们使用的Redfield模型表明，复杂的实现这种效果，通过调整网站III的能量通过其内部半胱氨酸残基的氧化还原状态。这一结果显示了色素蛋白质复合物如何利用电子振动耦合的量子力学来控制能量转移。
Photosynthetic species evolved to protect their light-harvesting apparatus from photoxidative damage driven by intracellular redox conditions or environmental conditions. The Fenna-Matthews-Olson (FMO) pigment-protein complex from green sulfur bacteria exhibits redox-dependent quenching behavior partially due to two internal cysteine residues. Here, we show evidence that a photosynthetic complex exploits the quantum mechanics of vibronic mixing to activate an oxidative photoprotective mechanism. We use two-dimensional electronic spectroscopy (2DES) to capture energy transfer dynamics in wild-type and cysteine-deficient FMO mutant proteins under both reducing and oxidizing conditions. Under reducing conditions, we find equal energy transfer through the exciton 4-1 and 4-2-1 pathways because the exciton 4-1 energy gap is vibronically coupled with a bacteriochlorophyll-a vibrational mode. Under oxidizing conditions, however, the resonance of the exciton 4-1 energy gap is detuned from the vibrational mode, causing excitons to preferentially steer through the indirect 4-2-1 pathway to increase the likelihood of exciton quenching. We use a Redfield model to show that the complex achieves this effect by tuning the site III energy via the redox state of its internal cysteine residues. This result shows how pigment-protein complexes exploit the quantum mechanics of vibronic coupling to steer energy transfer.