Proton care and relay in bio-relevant proton-coupled electron transfers – TAKE CARE

The association between electron transfer and proton transfer (PCET) has a long experimental and theoretical history in chemistry and biochemistry. Indeed it occurs in many electron transfer reactions, in radical chemistry and also plays a critical role in a wide range of biological processes, including enzyme reactions, photosynthesis and respiration as well as in chemical energy conversion and storage processes. In this later field, water splitting, proton and carbon dioxide reduction that all involve intimate PCET are among the holy grails of the 21st century chemistry.
In addressing the creation of a water-splitting catalyst, a recent discover has underlined several design constraints (Science, 2008, 321, 1072). One particular aspect is that the catalyst operates in water under ambient environmental conditions. This constraint leads to significant challenges. Indeed water is a poor proton acceptor under neutral conditions and due to the fact that activation of oxygen in water requires efficient PCET processes to reach the rate determining step corresponding to O-O bond formation, the creation of a water-splitting catalyst requires a proton acceptor to take care of the released protons. Moreover, except precious metal oxides, the best proton acceptor in neutral water is typically the catalyst itself and hence the protons produced from water splitting often promote corrosion of the catalyst. Consequently, a proton accepting base should be present and able to carry out the proton. Within that context, our proposal will focus on proton fate in PCET processes. In building our program we will take advantage of several results already obtained from our previous work on PCET for further studies of biomimicking metal-aqua complexes involved in catalytic processes. Of particular interest are the Mn complexes involved in the oxidation of water to oxygen in water oxidase system in Photosystem II or in the dismutation of superoxide anion into oxygen and hydrogen peroxide (Mn-superoxide dismutase). It could be emphasized that this last example will offer the opportunity to tackle another issue in the PCET area which is the question of the dichotomy between innersphere electron transfer vs. outersphere electron transfer in a PCET context. If water is too weak a base to trigger CPET in metal-aqua complexes, we have shown using several different and complementary experimental techniques (direct electrochemistry, photochemistry, redox catalysis, stopped-flow) that it may be able, in the absence of large buffer concentration and at acidic pH, to trigger a concerted oxidation of phenol thus establishing for the first time the crucial role of water in such concerted processes (PNAS, 2009, 106, 18143). This may have important implications in bio-catalysis since phenol is a ‘model’ for tyrosine, a cofactor in numerous biological processes where it is oxidized with the loss of a proton. Moreover, the efficient proton transfer to water, despite its poor basicity, is a striking feature that will be investigated on a fundamental point of view, i.e. in terms of intrinsic reactivity. Another goal of the present proposal is to compare intrinsic properties of water and other bases as proton acceptor. It is well known that PCET is intrinsically a quantum mechanical effect because both the electron and proton tunnel as a result of the overlap between the donor and acceptor wave functions. For this reason, PT distances are therefore confined to the hydrogen-bond length scale. However, the efficient proton transfer to water mentioned above opens the possibility of transferring efficiently proton over distance through water chain molecules. Long–distance electron and proton transfer or transport are indeed key-issues in a considerable number of natural systems.
We will explore the idea according to which this distance might be substantially increased by inserting a hydrogen-bond relay between the group being oxidized and the distant proton acceptor.