Sunlight is the ultimate energy source for the vast majority of life on earth, and photosynthetic organisms have evolved elegant machinery for its capture and utilization. Recent advances in nanotechnology are allowing humans to control matter on the scale of the biological machinery of life. As this field progresses, humans will have the ability to develop complex constructs that previously have been the secret of nature. Toward these efforts, a detailed knowledge of the bioenergetic processes of natural systems will provide fundamental design principles for the development of artificial systems. Conversely, knowledge gained from the study of artificial systems will improve our understanding of complex biological machinery.

In this work, a bioinspired system, composed of colloidal titanium dioxide nanoparticles surface modified with a photochemically active mimic of the photosystem II P680-tyrosine-histidine complex, undergoes photoinduced stepwise electron transfer coupled to proton motion at the phenolic site. Electron paramagnetic resonance studies reveal that injected electrons are localized on titanium dioxide following photoexcitation. At 80 K, the resulting holes are localized 95% on the phenol moiety and 5% on the porphyrin. At 4.2 K, 52% of the holes remain trapped on the porphyrin. The observed temperature dependence of the charge shift is attributed to restricted nuclear motion at low temperature and is reminiscent of the observation of a trapped high-energy state in the natural system. Electrochemical studies show that the phenoxyl/phenol couple of the model system is chemically reversible and thermodynamically capable of water oxidation. Studies under acidic and basic conditions provide clear evidence that an ionizable proton controls the electrochemical potential of the tyrosine-histidine mimic and that an exogenous base or acid can be used to generate a low-potential or high-potential mediator, respectively. However, the phenoxyl/phenoxide couple associated with the low-potential mediator is thermodynamically incapable of water oxidation, while the relay associated with the high-potential mediator is incapable of reducing an attached porphyrin. These studies provide insight regarding a mechanistic understanding for the role of the tyrosine-histidine complex in water oxidation and strategies for making use of hydrogen bonds to affect the coupling between proton and electron transfer in artificial systems.