On the antiquity of metalloenzymes and their substrates in bioenergetics.

Many metalloenzymes that inject and extract reducing equivalents at the beginning and the end of electron transport chains involved in chemiosmosis are suggested, through phylogenetic analysis, to have been present in the Last Universal Common Ancestor (LUCA). Their active centres are affine with the structures of minerals presumed to contribute to precipitate membranes produced on the mixing of hydrothermal solutions with the Hadean Ocean ~4 billion years ago. These mineral precipitates consist of transition element sulphides and oxides such as nickelian mackinawite ([Fe>Ni]2S2), a nickel-bearing greigite (~FeSS[Fe3NiS4]SSFe), violarite (~NiSS[Fe2Ni2S4]SSNi), a molybdenum bearing complex (~Mo(IV/VI)2Fe3S(0/2-)9) and green rust or fougerite (~[Fe(II)Fe(III)(OH)4](+)[OH](-)). They may be respectively compared with the active centres of Ni-Fe hydrogenase, carbon monoxide dehydrogenase (CODH), acetyl coenzyme-A synthase (ACS), the complex iron-sulphur molybdoenzyme (CISM) superfamily and methane monooxygenase (MMO). With the look of good catalysts - a suggestion that gathers some support from prebiotic hydrothermal experimentation - and sequestered by short peptides, they could be thought of as the original building blocks of proto-enzyme active centres. This convergence of the makeup of the LUCA-metalloenzymes with mineral structure and composition of hydrothermal precipitates adds credence to the alkaline hydrothermal (chemiosmotic) theory for the emergence of life, specifically to the possibility that the first metabolic pathway - the acetyl CoA pathway - was initially driven from either end, reductively from CO2 to CO and oxidatively and reductively from CH4 through to a methane thiol group, the two entities assembled with the help of a further thiol on a violarite cluster sequestered by peptides. By contrast, the organic coenzymes were entirely a product of the first metabolic pathways. This article is part of a Special Issue entitled: Metals in Bioenergetics and Biomimetics Systems. Published by Elsevier B.V.