The energetics of the reductive citric acid cycle in the pyrite-pulled surface metabolism in the early stage of evolution

The chemoautotrophic theory concerning the origin of life postulates that a central role is played in the prebiotic chemical machinery by a reductive citric acid cycle operating without enzymes. The crucial point in this scenario is the formation of pyrite from hydrogen sulfide and ferrous sulfide, a reaction suggested to be linked to endergonic reactions, making them exergonic. This mechanism is believed to provide the driving force for the cycle to operate as a carbon dioxide fixation network. The present paper criticizes the thermodynamic calculations and their presentation in the original version of the archaic reductive citric acid cycle [Wächtershäuser, 1990. Evolution of the first metabolic cycles. Proc. Natl Acad. Sci. USA 87, 200–204.]. The most significant differences between the Wächtershäuser hypothesis and the present proposal: Wächtershäuser did not consider individual reactions in his calculations. A particularly questionable feature is the involvement of seven molecules of pyrite which does not emerge as a direct consequence of the chemical reactions presented in the archaic reductive citric acid cycle. The involvement of a considerable number of sulfur-containing organic intermediates as building blocks is also disputed. In the new scheme of the cycle proposed here, less free energy is liberated than hypothesized by Wächtershäuser, but it has the advantages that the free energy changes for the individual reactions can be calculated, the number of pyrite molecules involved in the cycle is reduced, and fewer sulfur-containing intermediates are required for the cycle to operate. In combination with a plausible route for the anaplerotic reactions [Kalapos, 1997a. Possible evolutionary role of methylglyoxalase pathway: anaplerotic route for reductive citric acid cycle of surface metabolists. J. Theor. Biol. 188, 201–206.], this new presentation of the cycle assigns a special meaning to hydrogen sulfide formation in the early stage of biochemical evolution.