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The second law of thermodynamics leaves no doubt that life on planet Earth and its inherent substantial decrease in entropy is fundamentally based on mechanisms converting environmental free energy into the spatial and temporal order of metabolic processes. This argument holds for present life as much as it does for its very beginnings some 4 billion years ago. In this contribution, we try to strip down free energy conversion in extant life (known as "bioenergetics" to the biologists) to its basic principles with the aim to potentially retrodict the nature of the pre‐biotic precursor which drove life into existence. We demonstrate that these basic principles are deeply rooted in aqueous electrochemistry and strongly rely on inorganic redox compounds. The question of life's emergence, generally considered to fall into the realm of organic chemistry, should therefore rather be recognized as an electrochemical problem and its ultimate elucidation will need to strongly implicate the community of electrochemical scientists. [ABSTRACT FROM AUTHOR]

To link to full-text access for this article, visit this link: http://dx.doi.org/10.1016/j.tibs.2008.10.005 Byline: Anne-Lise Ducluzeau (1), Robert van Lis (1), Simon Duval (1), Barbara Schoepp-Cothenet (1), Michael J. Russell (2), Wolfgang Nitschke (1) Abstract: Evolutionary histories of enzymes involved in chemiosmotic energy conversion indicate that a strongly oxidizing substrate was available to the last universal common ancestor before the divergence of Bacteria and Archaea. According to palaeogeochemical evidence, O.sub.2 was not present beyond trace amounts on the early Earth. Based on recent phylogenetic, enzymatic and geochemical results, we propose that, in the earliest Archaean, nitric oxide (NO) and its derivatives nitrate and nitrite served as strongly oxidizing substrates driving the evolution of a bioenergetic pathway related to modern dissimilatory denitrification. Aerobic respiration emerged later from within this ancestral pathway via adaptation of the enzyme NO reductase to its new substrate, dioxygen. Author Affiliation: (1) Laboratoire de Bioenergetique et Ingenierie des Proteines, Centre National de la Recherche Scientifique UPR9036, IFR77, 31 chemin Joseph-Aiguier, 13402 Marseille Cedex 20, France (2) Planetary Science and Life Detection, Section 3220, MS:183-601, Jet Propulsion Laboratory, California Institute of Technology, 4800 Oak Grove Drive, Pasadena, CA 91109-8099, USA

Abstract Background Phylogenies of certain bioenergetic enzymes have proved to be useful tools for deducing evolutionary ancestry of bioenergetic pathways and their relationship to geochemical parameters of the environment. Our previous phylogenetic analysis of arsenite oxidase, the molybdopterin enzyme responsible for the biological oxidation of arsenite to arsenate, indicated its probable emergence prior to the Archaea/Bacteria split more than 3 billion years ago, in line with the geochemical fact that arsenite was present in biological habitats on the early Earth. Respiratory arsenate reductase (Arr), another molybdopterin enzyme involved in microbial arsenic metabolism, serves as terminal oxidase, and is thus situated at the opposite end of bioenergetic electron transfer chains as compared to arsenite oxidase. The evolutionary history of the Arr-enzyme has not been studied in detail so far. Results We performed a genomic search of genes related to arrA coding for the molybdopterin subunit. The multiple alignment of the retrieved sequences served to reconstruct a neighbor-joining phylogeny of Arr and closely related enzymes. Our analysis confirmed the previously proposed proximity of Arr to the cluster of polysulfide/thiosulfate reductases but also unravels a hitherto unrecognized clade even more closely related to Arr. The obtained phylogeny strongly suggests that Arr originated after the Bacteria/Archaea divergence in the domain Bacteria, and was subsequently laterally distributed within this domain. It further more indicates that, as a result of accumulation of arsenate in the environment, an enzyme related to polysulfide reductase and not to arsenite oxidase has evolved into Arr. Conclusion These findings are paleogeochemically rationalized by the fact that the accumulation of arsenate over arsenite required the increase in oxidation state of the environment brought about by oxygenic photosynthesis.