Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials
Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials
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DOI：
10.1073/pnas.1316156111
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发表时间：
2014-01-14
影响因子：
11.1
通讯作者：
Blumberger, Jochen
中科院分区：
文献类型：
--
作者：
Breuer, Marian;Rosso, Kevin M.;Blumberger, Jochen
从金属还原细菌到细胞外固体金属氧化物的电子转移的自然广泛的过程需要独特的生物分子机制优化的远程电子传输。为了有效地执行这一功能，微生物已经适应了多血红素c型细胞色素，以将血红素辅因子排列成协同跨越细胞包膜的导线，沿着沿着大于100埃的距离传输电子。生物纳米技术设备设计的意义和机会是不言而喻的。然而，在分子水平上，这些蛋白质如何使电子沿着它们的血红素线穿梭，有效地导航蛋白质内的交叉点和蛋白质间的界面，仍然是一个迄今为止无法实验的谜。为了阐明这一关键话题，我们进行了广泛的量子力学/分子力学模拟计算逐步血红素血红素电子转移速率在最近结晶的外膜十血红素细胞色素MtrF。通过求解电子跳跃的主方程，我们估计通过溶剂化MtrF的内在最大可能电子通量为10（4）-10（5）s（-1），与最近测量的相关多血红素蛋白质复合物MtrCAB的速率一致。有趣的是，我们的计算表明，通过MtrF的快速电子传输是血红素氧化还原电位和沿着线的电子耦合强度之间的明确相关性的结果：只有在电子连接良好的堆叠血红素对之间才发生螺旋上升步骤。这一观察结果表明，蛋白质进化到含有低电位血红素，而不会减慢电子流。这些发现是特别深刻的光的功能相关的外膜蛋白的明显保守的交错交叉血红素丝结构基序。
The naturally widespread process of electron transfer from metal reducing bacteria to extracellular solid metal oxides entails unique biomolecular machinery optimized for long-range electron transport. To perform this function efficiently, microorganisms have adapted multiheme c-type cytochromes to arrange heme cofactors into wires that cooperatively span the cellular envelope, transmitting electrons along distances greater than 100 angstrom. Implications and opportunities for bionanotechnological device design are self-evident. However, at the molecular level, how these proteins shuttle electrons along their heme wires, navigating intraprotein intersections and interprotein interfaces efficiently, remains a mystery thus far inaccessible to experiment. To shed light on this critical topic, we carried out extensive quantum mechanics/molecular mechanics simulations to calculate stepwise heme-to-heme electron transfer rates in the recently crystallized outer membrane deca-heme cytochrome MtrF. By solving a master equation for electron hopping, we estimate an intrinsic, maximum possible electron flux through solvated MtrF of 10(4)-10(5) s(-1), consistent with recently measured rates for the related multiheme protein complex MtrCAB. Intriguingly, our calculations show that the rapid electron transport through MtrF is the result of a clear correlation between heme redox potential and the strength of electronic coupling along the wire: thermodynamically uphill steps occur only between electronically well-connected stacked heme pairs. This observation suggests that the protein evolved to harbor low-potential hemes without slowing down electron flow. These findings are particularly profound in light of the apparently well-conserved staggered cross-heme wire structural motif in functionally related outer membrane proteins.