Kinetics of redox conversion at a gold electrode of water-insoluble ubiquinone (UQ(10)) and plastoquinone (PQ(9)) incorporated in supported phospholipid layers

doi:10.1016/S0022-0728(98)00076-X

Journal of Electroanalytical Chemistry

Volume 451, Issues 1–2, 1 July 1998, Pages 139-144

https://doi.org/10.1016/S0022-0728(98)00076-X Get rights and content

Abstract

The cyclic voltammetry of UQ₍₁₀₎ and PQ₍₉₎ incorporated in a supported lipid bilayer and reacting at a gold electrode is quantitatively analyzed assuming that the electrochemical process consists of a nine-member square scheme and using the approach developed earlier by Laviron. The striking change affecting the shape of the cathodic peak in the cyclic voltammograms when pH is increased from less than 7.5 to higher values reflects a shift from kinetic control of the cathodic process by the equivalent first electron exchange to kinetic control by the equivalent second electron exchange. Reasonable values are found for the thermodynamic and kinetic characteristics of the electrochemical process.

Introduction

The redox and physicochemical characteristics of polyisoprenic quinones have much significance in mitochondria and chloroplast electron transfer chains. The hydrophobicity of the polyisoprenic tail of physiological quinones, often consisting of more than seven isoprenic units, is so extreme that aqueous solutions of these quinones cannot be obtained in order to study their redox conversions at electrodes. The hydrophobicity of the polyisoprenic tail also endows the physiological quinones with a lipidic character which is responsible for their location in the phospholipid bilayers of cell membranes.

In several papers the redox characteristics of models of physiological quinones were investigated in organic solvents or in aquo-alcoholic solvent mixtures, in the absence and in the presence of protons 1, 2, 3, 4, 5, 6, 7. It is questionable, however, if the results obtained from non-aqueous solvent studies can be transposed to the membrane case, where, although the quinone is located in a lipidic environment, water and its ions are able to participate in the chemical steps involved in the redox conversion [8]. For this reason, various methods were used to introduce UQ₍₁₀₎ at the interface between water and a possibly modified electrode, either through direct adsorption 8, 9, 10, 11or incorporation into an alkanethiol [12]or a phospholipid [13]monolayer deposited on the electrode surface.

In a previous paper [14], we reported another example of possible observation of the redox conversions of water-insoluble ubiquinones and plastoquinones taking place at a gold electrode in such a way that water molecules are available for the redox center of the molecule, i.e. the quinone moiety, while a lipidic environment is available for the tail. However, we reported then only a description of the cyclic voltammograms. We did not carry out a detailed analysis of characteristics of the cathodic and anodic peaks and of their shifts and changes in shape depending on the pH of the surrounding buffered aqueous solution.

In the present paper we apply the approach published by Laviron 15, 16, 17in this journal to the nine-member square scheme involved in the electrochemical reduction of the quinone and oxidation of the hydroquinone to justify quantitatively the observed behavior. We confirm the occurrence of various reaction sequences depending on pH and some aspects of the thermodynamics of the system. It also enables us to achieve the kinetic characterization of the redox transformation from an electrochemical point of view.

Section snippets

Experimental

The aluminium oxide-coated gold electrodes were prepared as previously described 18, 19, 20. The alkyl silane (OTS) coating followed by direct fusion of unilamellar vesicles of lipids containing the polyisoprenic quinone and final quinone and lipid assays were also reported earlier [14].

The electrochemical measurements were carried out in an anaerobic cell fitted with the working electrode, a saturated KCl calomel reference electrode (SCE) and a platinum foil as the auxiliary electrode. The

Results

We used a technology developed for supported bilayers in which the modified electrode is specially designed to provide the template for the bilayer 18, 19, 20. The gold electrode is coated with a template made of a microporous film of aluminium oxide. The geometry of the template consists of an array of cylindrical pores oriented perpendicularly to the electrode surface (Fig. 1a). The first hydrophobic layer is produced by self-assembly of an alkyl silane (OTS) on aluminium oxide. The

The framework of the theoretical analysis

Using the same notations as Laviron 15, 16, 17, the nine-member square scheme involved in the electrochemical conversion of the UQ₍₁₀₎H₂/UQ₍₁₀₎ or PQ₍₉₎H₂/PQ₍₉₎ redox system is as shown in Fig. 4. The protonations are assumed to be at equilibrium, and the symmetry factors of all the individual electron transfers are assumed equal to 0.5. Then it can be shown [16]that the nine-member square scheme behaves as a simple process consisting of two successive one-electron exchanges, with apparent rate

Conclusion

The application of the quantitative approach developed by Laviron 15, 16, 17for the study of the nine-member square scheme enabled us to simulate the observed cyclic voltammetry of UQ₍₁₀₎ and PQ₍₉₎ incorporated in a supported lipid bilayer and reacting at a gold electrode. The main result is that such an approach justifies the striking change affecting the shape of the cathodic peak in the cyclic voltammograms when the pH is increased from less than 7.5 to higher values. This reflects a shift

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Experimentally, the formal potential Ef of both processes I and II is calculated as the midpoint between the potentials of the reduction and oxidation peaks, respectively, assuming a quasi-reversible behaviour of the redox system. This could seem a rough approximation but it is a standard procedure for estimating the formal potentials from cyclic voltammetric experiments involving these kinds of complex systems [9–15,29–32]. The estimation of Ef has been made from the values of peak potentials obtained at the low scan rates, to minimise their influence.
In this work biomimetic monolayers of a MGDG, monogalactosyldiacylglycerol, and DGDG, digalactosyldiacylglycerol mixture (MD), in a ratio close to that of the thylakoid membranes of oxygenic photosynthetic organisms, have been prepared. The lipid mixture incorporates plastoquinone-9 (PQ), that is the electron and proton shuttle of the photosynthetic reaction centres. The MD:PQ mixtures have been firstly studied using surface pressure-area isotherms. Langmuir-Blodgett (LB) films of those mixtures have been transferred onto a substrate forming a monolayer that mimics one of the bilayer sides of the thylakoid membranes. These monolayers have been characterized topographically and electrochemically. The results show the influence of PQ in the MD matrix and its partial expulsion when increasing the surface pressure, obtaining two main PQ positions in the MD matrix. The calculated apparent electron transfer rate constants indicate a different kinetic control for the reduction and the oxidation of the PQ/PQH₂ couple, being k_Rapp(I) = 0.7 · 10^− 6 s^− 1, k_Rapp(II) = 2.2 · 10^− 9 s^− 1, k_Oapp(I) = 7.4 · 10^− 4 s^− 1 and k_Oapp(II) = 5.2 · 10^− 5 s^− 1, respectively. The comparison of the different galactolipid:PQ systems that our group has studied is also presented, concluding that the PQ position in the galactolipid matrix can be tuned according to several controlled variables.
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The formal potential values for process I, Ef(I), obtained for the ITO–MGDG:UQ 5:1 and 10:1 systems (Table 2), are close to that obtained for process I in the ITO–UQ system [22] and therefore process I is correlated with the UQ molecules located in the lipid matrix with their heads in direct contact or in a short distance to the ITO surface. The most of the formal potentials observed by previous authors for the UQ redox processes confined on an electrode surface [8,9,19,27,43,47–50] are in the range between − 0.14 V and − 0.09 V vs. Ag/AgCl/3 M KCl at pH 7.4. These last values are less thermodynamically favourable than that observed in this work for process I, which is correlated with the higher availability of protons in our system.
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Kinetics of redox conversion at a gold electrode of water-insoluble ubiquinone (UQ(10)) and plastoquinone (PQ(9)) incorporated in supported phospholipid layers

Abstract

Introduction

Section snippets

Experimental

Results

The framework of the theoretical analysis

Conclusion

J. Biol. Chem.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

FEBS Lett.

Bioelectrochem. Bioenerg.

Bioelectrochem. Bioenerg.

Bioelectrochem. Bioenerg.

J. Electroanal. Chem.

Biophys. J.

Biophys. J.

J. Electroanal. Chem.

Kinetics of redox conversion at a gold electrode of water-insoluble ubiquinone (UQ₍₁₀₎) and plastoquinone (PQ₍₉₎) incorporated in supported phospholipid layers