Nitschke 2013 antiquity metalloenzymes BBA Metals first (original) (raw)
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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 afne 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] 2 S 2), a nickel-bearing greigite (~FeSS[Fe 3 NiS 4 ]SSFe), violarite (~NiSS[Fe 2 Ni 2 S 4 ]SSNi), a molybdenum bearing complex (~Mo IV/VI 2 Fe 3 S 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, specically to the possibility that the rst metabolic pathway – the acetyl CoA pathway – was initially driven from either end, reductively from CO 2 to CO and oxidatively and reductively from CH 4 through to a methane thiol group, the two entities assembled with the help of a further thiol on a violarite cluster seques-tered by peptides. By contrast, the organic coenzymes were entirely a product of the rst metabolic pathways. This article is part of a Special Issue entitled: Metals in Bioenergetics and Biomimetics Systems. Published by Elsevier B.V. It is the inorganic elements that bring organic chemistry to life David Garner
Journal of Molecular Evolution, 2009
Energised by the protonmotive force and with the intervention of inorganic catalysts, at base Life reacts hydrogen from a variety of sources with atmospheric carbon dioxide. It seems inescapable that life emerged to fulfil the same role (i.e., to hydrogenate CO 2) on the early Earth, thus outcompeting the slow geochemical reduction to methane. Life would have done so where hydrothermal hydrogen interfaced a carbonic ocean through inorganic precipitate membranes. Thus we argue that the first carbonfixing reaction was the molybdenum-dependent, protontranslocating formate hydrogenlyase system described by Andrews et al. (Microbiology 143:3633-3647, 1997), but driven in reverse. Alkaline on the inside and acidic and carbonic on the outside-a submarine chambered hydrothermal mound built above an alkaline hydrothermal spring of long duration-offered just the conditions for such a reverse reaction imposed by the ambient protonmotive force. Assisted by the same inorganic catalysts and potential energy stores that were to evolve into the active centres of enzymes supplied variously from ocean or hydrothermal system, the formate reaction enabled the rest of the acetyl coenzyme-A pathway to be followed exergonically, first to acetate, then separately to methane. Thus the two prokaryotic domains both emerged within the hydrothermal mound-the acetogens were the forerunners of the Bacteria and the methanogens were the forerunners of the Archaea.
The FEBS Journal
Hydrogen gas, H 2 , is generated in serpentinizing hydrothermal systems, where it has supplied electrons and energy for microbial communities since there was liquid water on Earth. In modern metabolism, H 2 is converted by hydrogenases into organically bound hydrides (H-), for example, the cofactor NADH. It transfers hydrides among molecules, serving as an activated and biologically harnessed form of H 2. In serpentinizing systems, minerals can also bind hydrides and could, in principle, have acted as inorganic hydride donors-possibly as a geochemical protoenzyme, a 'geozyme'-at the origin of metabolism. To test this idea, we investigated the ability of H 2 to reduce NAD + in the presence of iron (Fe), cobalt (Co) and nickel (Ni), metals that occur in serpentinizing systems. In the presence of H 2 , all three metals specifically reduce NAD + to the biologically relevant form, 1,4-NADH, with up to 100% conversion rates within a few hours under alkaline aqueous conditions at 40°C. Using Henry's law, the partial pressure of H 2 in our reactions corresponds to 3.6 mM, a concentration observed in many modern serpentinizing systems. While the reduction of NAD + by Ni is strictly H 2-dependent, experiments in heavy water (2 H 2 O) indicate that native Fe can reduce NAD + both with and without H 2. The results establish a mechanistic connection between abiotic and biotic hydride donors, indicating that geochemically catalysed, H 2-dependent NAD + reduction could have preceded the hydrogenase-dependent reaction in evolution. Abbreviations 1 H-NMR, proton nuclear magnetic resonance, an analytical method to characterise and quantify hydrogen-containing molecules; Co, cobalt; Fd ox /Fd red , oxidised/reduced ferredoxins; Fe, iron; LUCA, the last universal common ancestor, a theoretical cell based on phylogenetic reconstructions of the most conserved genetic setup between bacteria and archaea; NAD + /NADH, oxidised and reduced form of nicotinamide adenine dinucleotide; Ni, nickel.
5 Minerals and the Emergence of Life
Metals, Microbes, and Minerals - The Biogeochemical Side of Life, 2021
Metal-bearing minerals are an integral part of almost all "metabolism-first"-type scenarios for the emergence of life which consider that life is better defined by what it does than what it is made from. Since metals are formidable catalysts, these scenarios stipulate that early metabolic reactions (and prominently the reduction of CO2 to yield biomass) were performed by (mainly transition) metals contained in certain minerals. Metabolism-first scenarios stand in opposition to primordial soup hypotheses which envisage prebiotic synthesis of organic molecules as building blocks for life to be the salient feature enabling life to come into being. A critical analysis of the historical roots of these emergence of life hypotheses highlights fundamental inconsistencies prompting us to appeal to basic thermodynamic principles to provide rigorous guidelines for developing contradiction-free models. Combining these guidelines with our present-day understanding of biological energy conversion, arguably the process most fundamental to all life, strongly suggests an expansion of previous mineral-based scenarios to include processes converting environmental redox tensions into phosphate-grouptransfer disequilibria, i.e., the quintessential free energy converting mechanism of extant life. Based on their reported physicochemical and electrochemical properties, iron-(together with other transition metal-) based layered double oxyhydroxide (Fe-LDH) minerals such as fougerite are promising candidates to afford the required capacities and therefore may render previous mineral-based scenarios compliant with thermodynamic strictures.
Metalloproteins and the Pyrite-based Origin of Life: A Critical Assessment
Origins of Life and Evolution of Biospheres, 2011
We critically examine the proposal by Wächtershäuser (Prokaryotes 1:275–283, 2006a, Philos Trans R Soc Lond B Biol Sci 361: 787–1808, 2006b) that putative transition metal binding sites in protein components of the translation machinery of hyperthermophiles provide evidence of a direct relationship with the FeS clusters of pyrite and thus indicate an autotrophic origin of life in volcanic environments. Analysis
Inorganic Complexes Enabled the Onset of Life and Oxygenic Photosynthesis
Photosynthesis. Energy from the Sun, 2008
Mackinawite ([Fe>>Ni)S]), greigite (NiS 2 [Fe 4 S 4 ]S 2 Fe) and a tunnel manganite (CaMn 4 O 8 ) similar in structure to hollandite were minerals that enabled the onset of chemosynthesis and, later, of oxygenic photosynthesis -the two events to make the greatest impact at the surface of our planet. The inorganic complexes contributing to the growth of such minerals -([FeS 2 Fe]4H 2 O; [Fe 4 S 4 ] 2+/1+ ; [Fe 3 S 4 ] +1/0 ; NiFe 5 S 8 , CaMn 4 O 8 as well as HP 2 O 7
Iron Catalysis at the Origin of Life
AbstractIron–sulphur proteins are ancient and drive fundamental processes in cells, notably electron transfer and CO2 fixation. Iron–sulphur minerals with equivalent structures could have played a key role in the origin of life. However, the ‘iron–sulphur world’ hypothesis has had a mixed reception, with questions raised especially about the feasibility of a pyrites-pulled reverse Krebs cycle. Phylogenetics suggests that the earliest cells drove carbon and energy metabolism via the acetyl CoA pathway, which is also replete in Fe(Ni)S proteins. Deep differences between bacteria and archaea in this pathway obscure the ancestral state. These differences make sense if early cells depended on natural proton gradients in alkaline hydrothermal vents. If so, the acetyl CoA pathway diverged with the origins of active ion pumping, and ancestral CO2 fixation might have been equivalent to methanogens, which depend on a membrane-bound NiFe hydrogenase, energy converting hydrogenase. This uses the proton-motive force to reduce ferredoxin, thence CO2. The mechanism suggests that pH could modulate reduction potential at the active site of the enzyme, facilitating the difficult reduction of CO2 by H2. This mechanism could be generalised under abiotic conditions so that steep pH differences across semi-conducting Fe(Ni)S barriers drives not just the first steps of CO2 fixation to C1 and C2 organics such as CO, CH3SH and CH3COSH, but a series of similar carbonylation and hydrogenation reactions to form longer chain carboxylic acids such as pyruvate, oxaloacetate and α-ketoglutarate, as in the incomplete reverse Krebs cycle found in methanogens. We suggest that the closure of a complete reverse Krebs cycle, by regenerating acetyl CoA directly, displaced the acetyl CoA pathway from many modern groups. A later reliance on acetyl CoA and ATP eliminated the need for the proton-motive force to drive most steps of the reverse Krebs cycle. © 2017 The Authors IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 2017
Scientific Reports, 2020
Modern biological dependency on trace elements is proposed to be a consequence of their enrichment in the habitats of early life together with Earth’s evolving physicochemical conditions; the resulting metallic biological complement is termed the metallome. Herein, we detail a protocol for describing metallomes in deep time, with applications to the earliest fossil record. Our approach extends the metallome record by more than 3 Ga and provides a novel, non-destructive method of estimating biogenicity in the absence of cellular preservation. Using microbeam particle-induced X-ray emission (µPIXE), we spatially quantify transition metals and metalloids within organic material from 3.33 billion-year-old cherts of the Barberton greenstone belt, and demonstrate that elements key to anaerobic prokaryotic molecular nanomachines, including Fe, V, Ni, As and Co, are enriched within carbonaceous material. Moreover, Mo and Zn, likely incorporated into enzymes only after the Great Oxygenation ...
Scientific Reports, 2012
An evolutionary tree of key enzymes from the Complex-Iron-Sulfur-Molybdoenzyme (CISM) superfamily distinguishes ''ancient'' members, i.e. enzymes present already in the last universal common ancestor (LUCA) of prokaryotes, from more recently evolved subfamilies. The majority of the presented subfamilies and, as a consequence, the Molybdo-enzyme superfamily as a whole, appear to have existed in LUCA. The results are discussed with respect to the nature of bioenergetic substrates available to early life and to problems arising from the low solubility of molybdenum under conditions of the primordial Earth.