Beratan David N, Liu Chaoren, Migliore Agostino, Polizzi Nicholas F, Skourtis Spiros S, Zhang Peng, Zhang Yuqi
Department of Chemistry, ‡Department of Biochemistry and §Department of Physics, Duke University , Durham, North Carolina 27708, United States.
Acc Chem Res. 2015 Feb 17;48(2):474-81. doi: 10.1021/ar500271d. Epub 2014 Oct 13.
CONSPECTUS: The image is not the thing. Just as a pipe rendered in an oil painting cannot be smoked, quantum mechanical coupling pathways rendered on LCDs do not convey electrons. The aim of this Account is to examine some of our recent discoveries regarding biological electron transfer (ET) and transport mechanisms that emerge when one moves beyond treacherous static views to dynamical frameworks. Studies over the last two decades introduced both atomistic detail and macromolecule dynamics to the description of biological ET. The first model to move beyond the structureless square-barrier tunneling description is the Pathway model, which predicts how protein secondary motifs and folding-induced through-bond and through-space tunneling gaps influence kinetics. Explicit electronic structure theory is applied routinely now to elucidate ET mechanisms, to capture pathway interferences, and to treat redox cofactor electronic structure effects. Importantly, structural sampling of proteins provides an understanding of how dynamics may change the mechanisms of biological ET, as ET rates are exponentially sensitive to structure. Does protein motion average out tunneling pathways? Do conformational fluctuations gate biological ET? Are transient multistate resonances produced by energy gap fluctuations? These questions are becoming accessible as the static view of biological ET recedes and dynamical viewpoints take center stage. This Account introduces ET reactions at the core of bioenergetics, summarizes our team's progress toward arriving at an atomistic-level description, examines how thermal fluctuations influence ET, presents metrics that characterize dynamical effects on ET, and discusses applications in very long (micrometer scale) bacterial nanowires. The persistence of structural effects on the ET rates in the face of thermal fluctuations is considered. Finally, the flickering resonance (FR) view of charge transfer is presented to examine how fluctuations control low-barrier transport among multiple groups in van der Waals contact. FR produces exponential distance dependence in the absence of tunneling; the exponential character emerges from the probability of matching multiple vibronically broadened electronic energies within a tolerance defined by the rms coupling among interacting groups. FR thus produces band like coherent transport on the nanometer length scale, enabled by conformational fluctuations. Taken as a whole, the emerging context for ET in dynamical biomolecules provides a robust framework to design and interpret the inner workings of bioenergetics from the molecular to the cellular scale and beyond, with applications in biomedicine, biocatalysis, and energy science.
概述:图像并非事物本身。就如同油画中描绘的烟斗无法用于吸烟一样,液晶显示屏上呈现的量子力学耦合路径并不能传导电子。本综述的目的是探讨我们最近在生物电子转移(ET)和输运机制方面的一些发现,这些机制是在人们从危险的静态观点转向动态框架时出现的。过去二十年的研究将原子细节和大分子动力学引入了生物ET的描述中。第一个超越无结构方势垒隧穿描述的模型是路径模型,它预测了蛋白质二级基序以及折叠诱导的键间和空间隧穿间隙如何影响动力学。现在,显式电子结构理论经常被用于阐明ET机制、捕捉路径干扰以及处理氧化还原辅因子的电子结构效应。重要的是,蛋白质的结构采样有助于理解动力学如何改变生物ET的机制,因为ET速率对结构呈指数敏感。蛋白质运动是否会使隧穿路径平均化?构象波动是否会控制生物ET?能隙波动是否会产生瞬态多态共振?随着生物ET的静态观点逐渐消退,动态观点占据中心舞台,这些问题正变得可以解答。本综述介绍了生物能量学核心的ET反应,总结了我们团队在实现原子水平描述方面的进展,研究了热波动如何影响ET,提出了表征动力学对ET影响的指标,并讨论了在非常长(微米尺度)的细菌纳米线中的应用。考虑了在热波动情况下结构效应在ET速率上的持续性。最后,提出了电荷转移的闪烁共振(FR)观点,以研究波动如何控制范德华接触中多个基团之间的低势垒输运。在没有隧穿的情况下,FR产生指数距离依赖性;这种指数特性源于在由相互作用基团之间的均方根耦合定义的容差内匹配多个振动加宽电子能量的概率。因此,FR在纳米长度尺度上产生类似能带的相干输运,这是由构象波动实现的。总体而言,动态生物分子中ET的新兴背景为从分子到细胞尺度及更广泛范围设计和解释生物能量学的内部运作提供了一个强大的框架,在生物医学、生物催化和能源科学中有应用。
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