Interprotein electron transfer from cytochromec₂to photosynthetic reaction center: Tunneling across an aqueous interface

Abstract

Interprotein electron transfer (ET) reactions play an important role in biological energy conversion processes. One of these reactions, the ET between cytochrome c2 (cyt) and reaction center from photosynthetic bacteria, is the focus of this theoretical study. The changes in the ET rate constant at fixed distances during the association process were calculated as the cyt moved from the electrostatically stabilized encounter complex to the bound state having short range van der Waals contacts in the tunneling region. Multiple conformations of the protein were generated by molecular dynamics simulations including explicit water molecules. For each of these conformations, the ET rate was calculated by using the Pathways model. The ET rate increased smoothly as the cyt approached from the encounter complex to the bound state, with a tunneling decay factor ␤ ‫؍‬ 1.1 Å ؊1 . This relatively efficient coupling between redox centers is due to the ability of interfacial water molecules to form multiple strong hydrogen bonding pathways connecting tunneling pathways on the surfaces of the two proteins. The ET rate determined for the encounter complex ensemble of states is only about a factor of 100 slower than that of the bound state ( ‫؍‬ 100 s, compared with 1 s), because of fluctuations of the cyt within the encounter complex ensemble through configurations having strong tunneling pathways. The ET rate for the encounter complex is in agreement with rates observed in mutant reaction centers modified to remove shortrange hydrophobic interactions, suggesting that in this case, ET occurs within the solvent-separated, electrostatically stabilized encounter complex.encounter complex ͉ protein complex ͉ tunneling pathways E lectron transfer (ET) reactions play vital roles in biological systems. Intraprotein ET through redox cofactors bound within membrane proteins and interprotein ET between cofactors in different protein molecules provide the basis for energy conversion processes such as photosynthesis and respiration. The past few decades has seen tremendous growth in the development of reliable molecular-level theories and models for intramolecular biological ET reactions (for reviews, see refs. 1-7). However, relatively limited attention has been devoted to interprotein ET. These ET reactions are more complex, involving an additional association step needed to bring the two proteins into position for ET to occur.In this article, we investigate the interprotein ET reaction between the photosynthetic reaction center (RC) and the mobile electron carrier protein, cytochrome c 2 (cyt), that are part of the ET cycle in photosynthetic bacteria (1,8). The RC captures light energy by intraprotein ET to form an oxidized primary donor (bacteriochlorophyll dimer, D) and a reduced acceptor quinone (Q). The cyt transfers electrons to the oxidized primary donor in the RC as part of the light-induced ET chain that is coupled to proton pumping and ATP formation. Extensive experimental studies have been performed to understand this ET reacti...

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