On the antiquity of metalloenzymes and their substrates in bioenergetics

Abstract

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.

The inevitable journey to being

“…A secondary acidulous ocean current bearing the oxidants is convectively driven by heat emanating from the mound and also pulled upward by entrainment in a manner comparable to a carburettor so that the reductants-delivered at a similar rate to the oxidants-are partially oxidized to organic intermediates [8,26,46]. Reactions are catalysed by the (dislocated) surfaces of transition metal sulfides or in the interlayers of green rust acting here as a di-iron methane monooxygenase [19,126]. The specific model engines argued here to have driven the first metabolic pathway are (i) electron bifurcation on Mo-sulfides reduced by H 2 in a two-electron reaction but ejecting these electrons in a gated manner towards a high potential acceptor (such as nitrate or nitrite) and a low potential iron -nickel -sulfur-containing mineral such as violarite [19,104,127].…”

“…Mixed valence iron (nickel) sulfides (mackinawite and the thiospinels, greigite and violarite) and iron oxyhydroxides (green rust) dominated the mineralogy [128 -136]. It is worth noting in passing that mackinawite, violarite and greigite have structures generally affine with the active centres of hydrogenase (CO dehydrogenase (CODH) and acetyl coenzyme-A synthase (ACS)), whereas green rust has a similar structure to di-iron methane monooxygenase [19,126,[133][134][135][136].…”

“…This well-ordered hydrothermal effluent is driven convectively to the ocean floor where, on interaction with mildly acidic ocean water, porous mounds comprising iron -magnesium hydroxides and silicates, iron-nickel-cobalt -molybdenum sulfides and ephemeral iron -calcium -magnesium carbonates are precipitated [24,25,99]. We argue here that some of the marginal compartments, subjected to redox, pH and thermal gradients, assemble natural engines to dissipate these disequilibria while driving endergonic (anti-entropic) reactions: (i) a nickel/iron/molybdenum sulfide engine reducing CO 2 to CO, (ii) an electron bifurcating mixed valence molybdenum-bearing iron sulfide composite engine dissipates redox energy through the reduction of nitrite while oxidizing hydrothermal methane and reducing oceanic carbon dioxide, resulting in the generation of activated acetate [46], (iii) a pyrophosphatase engine comprising green rust interlayers [100,101] that clamp contiguous orthophosphates (2 Â HPO 4 22 or Pi 22 ) in a natural metal ion mediated binding site where they condense, only to be released in the proton flux [19].…”

“…In these cases, driving gradients of relatively modest strength can be sufficient to initiate dissipative engines and keep them fed and growing. An example of this as it applies to the emergence of life are the inorganic prebiotic mineral structures involving iron sulfides, dosed with nickel, cobalt and molybdenum and the iron oxyhydroxides, so similar to the active centres of the metalloenzymes, that played a vital role in the first metabolic pathways [19][20][21].…”

Evolution of ribozymes in the presence of a mineral surface

“…Mineral surfaces can support several processes that may be exploited by emerging life (Hazen and Sverjensky 2010) including the selective sorption (Franchi et al 2003), concentration, protection (Biondi et al 2007b), organization (Hanczyc et al 2003;Konnyu et al 2015;Shay et al 2015), and chemical transformation (Huang and Ferris 2006) of organic molecules. Additionally, similarities between some bioinorganic structures and mineral surfaces suggest that metabolic functions in emerging life occurred on mineral surfaces (Nitschke et al 2013). It is therefore important to address the role of inorganic structures when considering the processes involved in the origin(s) and early evolution of life.…”