Solid-state electron transport via cytochrome c depends on electronic coupling to electrodes and across the protein (original) (raw)
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The Journal of Physical Chemistry B, 2013
Nonexponential distance dependence of the apparent electron-transfer (ET) rate has been reported for a variety of redox proteins immobilized on biocompatible electrodes, thus posing a physicochemical challenge of possible physiological relevance. We have recently proposed that this behavior may arise not only from the structural and dynamical complexity of the redox proteins but also from their interplay with strong electric fields present in the experimental setups and in vivo (J. Am Chem. Soc. 2010, 132, 5769−5778). Therefore, protein dynamics are finely controlled by the energetics of both specific contacts and the interaction between the protein's dipole moment and the interfacial electric fields. In turn, protein dynamics may govern electron-transfer kinetics through reorientation from low to high donor−acceptor electronic coupling orientations. Here we present a combined computational and experimental study of WT cytochrome c and the surface mutant K87C adsorbed on electrodes coated with self-assembled monolayers (SAMs) of varying thickness (i.e., variable strength of the interfacial electric field). Replacement of the positively charged K87 by a neutral amino acid allowed us to disentangle protein dynamics and electron tunneling from the reaction kinetics and to rationalize the anomalous distance dependence in terms of (at least) two populations of distinct average electronic couplings. Thus, it was possible to recover the exponential distance dependence expected from ET theory. These results pave the way for gaining further insight into the parameters that control protein electron transfer.
Single-Molecule Mapping of Long-range Electron Transport for a Cytochrome b 562 Variant
Nano letters, 2011
Cytochrome b 562 was engineered to introduce a cysteine residue at a surface-exposed position to facilitate direct selfassembly on a Au(111) surface. The confined protein exhibited reversible and fast electron exchange with a gold substrate over a distance of 20 Å between the heme redox center and the gold surface, a clear indication that a long-range electron-transfer pathway is established. Electrochemical scanning tunneling microscopy was used to map electron transport features of the protein at the single-molecule level. Tunneling resonance was directly imaged and apparent molecular conductance was measured, which both show strong redox-gated effects. This study has addressed the first case of heme proteins and offered new perspectives in singlemolecule bioelectronics.
Electric-field effects on the interfacial electron transfer and protein dynamics of cytochrome c
Journal of Electroanalytical Chemistry, 2011
Time-resolved surface enhanced resonance Raman and surface enhanced infrared absorption spectroscopy have been employed to study the interfacial redox process of cytochrome c (Cyt-c) immobilised on various metal electrodes coated with self-assembled monolayers (SAMs) of carboxyl-terminated mercaptanes. The experiments, carried out with Ag, Au and layered Au-SAM-Ag electrodes, afford apparent heterogeneous electron transfer constants (k relax ) that reflect the interplay between electron tunnelling, redox-linked protein structural changes, protein re-orientation, and hydrogen bond re-arrangements in the protein and in the protein/SAM interface. It is shown that the individual processes are affected by the interfacial electric field strength that increases with decreasing thickness of the SAM and increasing difference between the actual potential and the potential of zero-charge. At thick SAMs of mercaptanes including 15 methylene groups, electron tunnelling (k ET ) is the rate-limiting step. Pronounced differences for k ET and its overpotential-dependence are observed for the three metal electrodes and can be attributed to the different electric-field effects on the free-energy term controlling the tunnelling rate. With decreasing SAM thickness, electron tunnelling increases whereas protein dynamics is slowed down such that for SAMs including less than 10 methylene groups, protein re-orientation becomes rate-limiting, as reflected by the viscosity dependence of k relax . Upon decreasing the SAM thickness from 5 to 1 methylene group, an additional H/D kinetic isotope effect is detected indicating that at very high electric fields rearrangements of the interfacial or intra-protein hydrogen bond networks limit the rate of the overall redox process.
Proteins as Electronic Materials: Electron Transport through Solid-State Protein Monolayer Junctions
Journal of the American Chemical Society, 2010
Electron transfer (ET) through proteins, a fundamental element of many biochemical reactions, has been studied intensively in solution. We report the results of electron transport (ETp) measurements across proteins, sandwiched between two solid electrodes with a long-range goal of understanding in how far protein properties are expressed (and can be utilized) in such a configuration. While most such studies to date were conducted with one or just a few molecules in the junction, we present the high yield, reproducible preparation of large area monolayer junctions of proteins from three different families: Azurin (Az), a blue-copper ET protein, Bacteriorhodopsin (bR), a membrane protein-chromophore complex with a proton pumping function, and Bovine Serum Albumin (BSA). Surprisingly, the currentvoltage (I-V) measurements on such junctions, which are highly reproducible, show relatively minor differences between Az and bR, even though the latter lacks a known ET function. ETp across both Az and bR is much more efficient than across BSA, but also for the latter the currents are still high, and the decay coefficients too low to be consistent with coherent tunneling. Rather, inelastic hopping is proposed to dominate ETp in these junctions. Other features such as asymmetrical I-V curves and distinct behavior of different proteins can be viewed as molecular signatures in the solid-state conductance.
Electron transfer in cytochrome c depends upon the structure of the intervening medium
Structure, 1994
Background: Long-distance electron-transfer (ET) reactions through proteins are involved in a great many biochemical processes; however, the way in which the protein structure influences the rates of these reactions is not well understood. We have therefore measured the rates of intramolecular ET from the ferroheme to a bis(2,2'-bipyridine)imidazoleruthenium(II) acceptor at histidine 39 or 54 in derivatives of yeast iso-l-cytochrome c, and studied the effect of an asparagine to isoleucine mutation at position 52, a residue situated between the heme and the electron acceptor. Results: The Fe 2 +-Ru 3 + rate constants demonstrate that residue 52 affects ET from the heme to His54 (Ile52 >Asn52), but not to His39 (Ile52 = Asn52). The enhanced Fe 2 +-Ru 3 + (His54) electronic coupling for the N52I/K54H protein is in good agreement with cr-tunneling calculations, which predict the length of the ET pathways between the heme and His54. Conclusion: The structure of the intervening medium between the heme and electron acceptors at the protein surface influences the donor-acceptor couplings in cytochrome c.
Langmuir, 2006
Cytochrome c was electrostatically immobilized onto a COOH-terminated alkanethiol self-assembled monolayer (SAM) on a gold electrode at ionic strengths of less than 40 mM. Scanning electrochemical microscopy (SECM) was used to simultaneously measure the electron transfer (ET) kinetics of the bimolecular ET between a solution-based redox mediator and the immobilized protein and the tunneling ET between the protein and the underlying gold electrode. Approach curves were recorded with ferrocyanide as a mediator at different coverages of cytochrome c and at different substrate potentials, allowing the measurement of k BI) 2 × 10 8 mol-1 cm 3 s-1 for the bimolecular ET and k°) 15 s-1 for the tunneling ET. The kinetics of ET was also found to depend on the immobilization conditions of cytochrome c: covalent attachment gave slightly slower tunneling ET values, and a mixed CH 3 /COOH-terminated ML gave faster tunneling ET rates. This is consistent with previous studies and is believed to be related to the degree of mobility of cyt c in its binding configuration and its orientation with respect to the underlying electrode surface.
Scientific reports, 2016
Enzymes in biology's energy chains operate with low energy input distributed through multiple electron transfer steps between protein active sites. The general challenge of biological design is how to lower the activation barrier without sacrificing a large negative reaction free energy. We show that this goal is achieved through a large polarizability of the active site. It is polarized by allowing a large number of excited states, which are populated quantum mechanically by electrostatic fluctuations of the protein and hydration water shells. This perspective is achieved by extensive mixed quantum mechanical/molecular dynamics simulations of the half reaction of reduction of cytochrome c. The barrier for electron transfer is consistently lowered by increasing the number of excited states included in the Hamiltonian of the active site diagonalized along the classical trajectory. We suggest that molecular polarizability, in addition to much studied electrostatics of permanent ch...
Large scale domain movement in cytochrome bc 1: a new device for electron transfer in proteins
Trends in Biochemical Sciences, 2001
Cytochrome bc 1 of most bacteria and mitochondria, and the analogous cytochrome b 6 f of chloroplasts and cyanobacteria, are key components of respiratory and photosynthetic electron transport chains 1-3 . These evolutionarily conserved energy transducing enzymes, generally known as cytochrome bc complexes, transfer electrons (e − s) from a hydroquinone (QH 2 ) derivative (ubi-, mena-or plastohydroquinone) to a c-type cytochrome or plastocyanin, and contribute to the generation of an electrochemical proton [H + ] gradient, which subsequently drives ATP synthesis, and ion and metabolite transport. Unlike the succinate dehydrogenases and some hydroquinone oxidases, which contribute only to the formation of a pH gradient, cytochrome bc 1 also transfers electrons across the membrane, thereby generating an electrical membrane potential. Thus, this enzyme contributes both to the ∆pH and ∆Ψ components of the proton motive force (∆µH + ) 4 . The first idea about how cytochrome bc 1 generated ∆µH + was presented by Wikström and Berden almost 30 years ago 5 . This was followed by the breakthrough model of Peter Mitchell, called the protonmotive Q-cycle 6 . However, even today, the mechanism of action of the catalytic events within cytochrome bc 1 is not completely understood.