On the origin of photophosphorylation

A model based on quinol phosphates is proposed for the origin of photophosphorylation. This model is divided into three time periods. In the early period, when the primitive earth was under reducing conditions, quinol phosphates were produced through quinol radical intermediates formed by the activation of hydroquinones with ultraviolet light. Phosphorylation of a number of acceptor molecules including inorganic orthophosphate and adenosine diphosphate occurred when quinol phosphate was oxidized by Fe⁺³ or a water soluble iron-sulfur complex. After the appearance of a rudimentary ozone layer (middle period), ultraviolet light was no longer an important factor in primordial chemistry. Quinol phosphates were then produced by visible light activation of porphyrin-quinone charge transfer complexes. In the presence of light, electrons from H₂S, H₂ and several reduced organic compounds were transfered through the porphyrin to quinone yielding the quinol radical. Again, quinol phosphate was produced from breakdown of the free radical. Phosphorylation of a number of acceptor molecules was achieved when quinol phosphates were oxidized by the iron-sulfur complexes. Evolutionary pressure to increase the efficiency of these reactions resulted in the electron donor-porphyrin-quinone-iron-sulfur complex becoming more lipophilic and thus associated with the protomembrane of the evolving protocell. In the late period the protomembrane became more sophisticated and quinone was replaced as the primary electron acceptor in the photoprocess by one of the iron-sulfur complexes originally present as oxidizing agents for the quinol phosphates. Quinones eventually lost their role as phosphorylating agents and became only electron and proton shuttles in the evolving electron transport chain. The protocell evolved the ability to use water as the electron donor as the relative roles of iron and quinone in the photoprocess switched.