Dataset Information

Fast proton-coupled electron transfer observed for a high-fidelity structural and functional [2Fe-2S] Rieske model.

ABSTRACT: Rieske cofactors have a [2Fe-2S] cluster with unique {His2Cys2} ligation and distinct Fe subsites. The histidine ligands are functionally relevant, since they allow for coupling of electron and proton transfer (PCET) during quinol oxidation in respiratory and photosynthetic ET chains. Here we present the highest fidelity synthetic analogue for the Rieske [2Fe-2S] cluster reported so far. This synthetic analogue 5(x-) emulates the heteroleptic {His2Cys2} ligation of the [2Fe-2S] core, and it also serves as a functional model that undergoes fast concerted proton and electron transfer (CPET) upon reaction of the mixed-valent (ferrous/ferric) protonated 5H(2-) with TEMPO. The thermodynamics of the PCET square scheme for 5(x-) have been determined, and three species (diferric 5(2-), protonated diferric 5H(-), and mixed-valent 5(3-)) have been characterized by X-ray diffraction. pKa values for 5H(-) and 5H(2-) differ by about 4 units, and the reduction potential of 5H(-) is shifted anodically by about +230 mV compared to that of 5(2-). While the N-H bond dissociation free energy of 5H(2-) (60.2 ± 0.5 kcal mol(-1)) and the free energy, ?G°CPET, of its reaction with TEMPO (-6.3 kcal mol(-1)) are similar to values recently reported for a homoleptic {N2/N2}-coordinated [2Fe-2S] cluster, CPET is significantly faster for 5H(2-) with biomimetic {N2/S2} ligation (k = (9.5 ± 1.2) × 10(4) M(-1) s(-1), ?H(‡) = 8.7 ± 1.0 kJ mol(-1), ?S(‡) = -120 ± 40 J mol(-1) K(-1), and ?G(‡) = 43.8 ± 0.3 kJ mol(-1) at 293 K). These parameters, and the comparison with homoleptic analogues, provide important information and new perspectives for the mechanistic understanding of the biological Rieske cofactor.

SUBMITTER: Albers A

PROVIDER: S-EPMC3985845 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Fast proton-coupled electron transfer observed for a high-fidelity structural and functional [2Fe-2S] Rieske model.

Albers Antonia A Demeshko Serhiy S Dechert Sebastian S Saouma Caroline T CT Mayer James M JM Meyer Franc F

Journal of the American Chemical Society 20140226 10

Rieske cofactors have a [2Fe-2S] cluster with unique {His2Cys2} ligation and distinct Fe subsites. The histidine ligands are functionally relevant, since they allow for coupling of electron and proton transfer (PCET) during quinol oxidation in respiratory and photosynthetic ET chains. Here we present the highest fidelity synthetic analogue for the Rieske [2Fe-2S] cluster reported so far. This synthetic analogue 5(x-) emulates the heteroleptic {His2Cys2} ligation of the [2Fe-2S] core, and it also ...[more]

PMID: 24506804

Similar Datasets

Project description:The Rieske protein component of the cytochrome bc complex contains a [2Fe-2S] cluster ligated by two cysteines and two histidines. We report here the pK(a) values of each of the imidazole rings of the two ligating histidines (His134 and His154) in the oxidized and reduced states of the Rieske protein from Thermus thermophilus (TtRp) as determined by NMR spectroscopy. Knowledge of these pK(a) values is of critical interest because of their pertinence to the mechanism of electron and proton transfer in the bifurcated Q-cycle. Although we earlier had observed the pH dependence of a (15)N NMR signal from each of the two ligand histidines in oxidized TtRp (Lin, I. J.; Chen, Y.; Fee, J. A.; Song, J.; Westler, W. M.; Markley, J. L. J. Am. Chem. Soc. 2006, 128, 10672-10673), the strong paramagnetism of the [2Fe-2S] cluster prevented the assignment of these signals by conventional methods. Our approach here was to take advantage of the unique histidine-leucine (His134-Leu135) sequence and to use residue-selective labeling to establish a key sequence-specific assignment, which was then extended. Analysis of the pH dependence of assigned (13)C', (13)C(alpha), and (15)N(epsilon2) signals from the two histidine cluster ligands led to unambiguous assignment of the pK(a) values of oxidized and reduced TtRp. The results showed that the pK(a) of His134 changes from 9.1 in oxidized to approximately 12.3 in reduced TtRp, whereas the pK(a) of His154 changes from 7.4 in oxidized to approximately 12.6 in reduced TtRp. This establishes His154, which is close to the quinone when the Rieske protein is in the cytochrome b site, as the residue experiencing the remarkable redox-dependent pK(a) shift. Secondary structural analysis of oxidized and reduced TtRp based upon our extensive chemical shift assignments rules out a large conformational change between the oxidized and reduced states. Therefore, TtRp likely translocates between the cytochrome b and cytochrome c sites by passive diffusion. Our results are most consistent with a mechanism involving the coupled transfer of an electron and transfer of the proton across the hydrogen bond between the hydroquinone and His154 at the cytochrome b site.

Project description:Designing molecular platforms for controlling proton and electron movement in artificial photosynthetic systems is crucial to efficient catalysis and solar energy conversion. The transfer of both protons and electrons during a reaction is known as proton-coupled electron transfer (PCET) and is used by nature in myriad ways to provide low overpotential pathways for redox reactions and redox leveling, as well as to generate bioenergetic proton currents. Herein, we describe theoretical and electrochemical studies of a series of bioinspired benzimidazole-phenol (BIP) derivatives and a series of dibenzimidazole-phenol (BI2P) analogs with each series bearing the same set of terminal proton-accepting (TPA) groups. The set of TPAs spans more than 6 pK a units. These compounds have been designed to explore the role of the bridging benzimidazole(s) in a one-electron oxidation process coupled to intramolecular proton translocation across either two (the BIP series) or three (the BI2P series) acid/base sites. These molecular constructs feature an electrochemically active phenol connected to the TPA group through a benzimidazole-based bridge, which together with the phenol and TPA group form a covalent framework supporting a Grotthuss-type hydrogen-bonded network. Infrared spectroelectrochemistry demonstrates that upon oxidation of the phenol, protons translocate across this well-defined hydrogen-bonded network to a TPA group. The experimental data show the benzimidazole bridges are non-innocent participants in the PCET process in that the addition of each benzimidazole unit lowers the redox potential of the phenoxyl radical/phenol couple by 60 mV, regardless of the nature of the TPA group. Using a series of hypothetical thermodynamic steps, density functional theory calculations correctly predicted the dependence of the redox potential of the phenoxyl radical/phenol couple on the nature of the final protonated species and provided insight into the thermodynamic role of dibenzimidazole units in the PCET process. This information is crucial for developing molecular "dry proton wires" with these moieties, which can transfer protons via a Grotthuss-type mechanism over long distances without the intervention of water molecules.

Dataset Information

Fast proton-coupled electron transfer observed for a high-fidelity structural and functional [2Fe-2S] Rieske model.

Publications

Fast proton-coupled electron transfer observed for a high-fidelity structural and functional [2Fe-2S] Rieske model.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure