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Hydrogen gas, H2, 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, H2 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 H2. 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 H2 to reduce NAD+ in the presence of iron (Fe), cobalt (Co) and nickel (Ni), metals that occur in serpentinizing systems. In the presence of H2, 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 H2 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 H2-dependent, experiments in heavy water (2H2O) indicate that native Fe can reduce NAD+ both with and without H2. The results establish a mechanistic connection between abiotic and biotic hydride donors, indicating that geochemically catalysed, H2-dependent NAD+ reduction could have preceded the hydrogenase-dependent reaction in evolution.

The metabolism of cells contains evidence reflecting the process by which they arose. Here, we have identified the ancient core of autotrophic metabolism encompassing 404 reactions that comprise the reaction network from H2, CO2, and ammonia (NH3) to amino acids, nucleic acid monomers, and the 19 cofactors required for their synthesis. Water is the most common reactant in the autotrophic core, indicating that the core arose in an aqueous environment. Seventy-seven core reactions involve the hydrolysis of high-energy phosphate bonds, furthermore suggesting the presence of a non-enzymatic and highly exergonic chemical reaction capable of continuously synthesizing activated phosphate bonds. CO2 is the most common carbon-containing compound in the core. An abundance of NADH and NADPH-dependent redox reactions in the autotrophic core, the central role of CO2, and the circumstance that the core’s main products are far more reduced than CO2 indicate that the core arose in a highly reducing environment. The chemical reactions of the autotrophic core suggest that it arose from H2, inorganic carbon, and NH3 in an aqueous environment marked by highly reducing and continuously far from equilibrium conditions. Such conditions are very similar to those found in serpentinizing hydrothermal systems.

Life as we know it would not exist without water. However, water molecules not only serve as a solvent and reactant but can also promote hydrolysis, which counteracts the formation of essential organic molecules. This conundrum constitutes one of the central issues in origin of life. Hydrolysis is an important part of energy metabolism for all living organisms but only because, inside cells, it is a controlled reaction. How could hydrolysis have been regulated under prebiotic settings? Lower water activities possibly provide an answer: geochemical sites with less free and more bound water can supply the necessary conditions for protometabolic reactions. Such conditions occur in serpentinising systems, hydrothermal sites that synthesise hydrogen gas via rock-water interactions. Here, we summarise the parallels between biotic and abiotic means of controlling hydrolysis in order to narrow the gap between biochemical and geochemical reactions and briefly outline how hydrolysis could even have played a constructive role at the origin of molecular self-organisation.

Carbon dioxide enters metabolism via six known CO 2 fixation pathways, of which only one is linear, exergonic in the direction of CO 2‐assimilation, and present in both bacterial and archaeal anaerobes – the Wood‐Ljungdahl (WL) or reductive acetyl‐CoA pathway. Carbon monoxide (CO) plays a central role in the WL pathway as an energy rich intermediate. Here, we scan the major biochemical reaction databases for reactions involving CO and CO 2. We identified 415 reactions corresponding to enzyme commission (EC) numbers involving CO 2, which are non‐randomly distributed across different biochemical pathways. Their taxonomic distribution, reversibility under physiological conditions, cofactors and prosthetic groups are summarized. In contrast to CO 2, only 15 reaction classes involving CO were detected. Closer inspection reveals that CO interfaces with metabolism and the carbon cycle at only two enzymes: anaerobic carbon monoxide dehydrogenase (CODH), a Ni‐ and Fe‐containing enzyme that generates CO for CO 2 fixation in the WL pathway, and aerobic CODH, a Mo‐ and Cu‐containing enzyme that oxidizes environmental CO as an electron source. The CO‐dependent reaction of the WL pathway involves carbonyl insertion into a methyl carbon‐nickel at the Ni‐Fe‐S A‐cluster of acetyl‐CoA synthase (ACS). It appears that no alternative mechanisms to the CO‐dependent reaction of ACS have evolved in nearly 4 billion years, indicating an ancient and mechanistically essential role for CO at the onset of metabolism.

Molecular hydrogen is an ancient source of energy and electrons. Anaerobic autotrophs that harness the H2/CO2 redox couple harbour ancient biochemical traits that trace back to the universal common ancestor. Aspects of their physiology, including the abundance of transition metals, radical reaction mechanisms, and their main exergonic bioenergetic reactions, forge links between ancient microbes and geochemical reactions at hydrothermal vents. The midpoint potential of H2 however requires anaerobes that reduce CO2 with H2 to use flavin based electron bifurcation — a mechanism to conserve energy as low potential reduced ferredoxins via soluble proteins — for CO2 fixation. This presents a paradox. At the onset of biochemical evolution, before there were proteins, how was CO2 reduced using H2? FeS minerals alone are probably not the solution, because biological CO2 reduction is a two electron reaction. Physiology can provide clues. Some acetogens and some methanogens can grow using native iron (Fe0) instead of H2 as the electron donor. In the laboratory, Fe0 efficiently reduces CO2 to acetate and methanol. Hydrothermal vents harbour awaruite, Ni3Fe, a natural compound of native metals. Native metals might have been the precursors of electron bifurcation in biochemical evolution.

Microorganisms living in hydrothermal vents that emit carbon dioxide gas provide a striking example of metabolic finesse. This pathway sheds light on microbial ecology in extreme environments and offers clues to early life on Earth. Mechanism used by microbes to reverse the tricarboxylic acid cycle found.

Hydrogen gas, H2, is generated in alkaline hydrothermal vents from reactions of iron containing minerals with water during a geological process called serpentinization. It has been a source of electrons and energy since there was liquid water on the early Earth, and it fuelled early anaerobic ecosystems in the Earth’s crust1–3. H2is the electron donor for the most ancient route of biological CO2fixation, the acetyl-CoA (or Wood-Ljungdahl) pathway, which unlike any other autotrophic pathway simultaneously supplies three key requirements for life: reduced carbon in the form of acetyl groups, electrons in the form of reduced ferredoxin, and ion gradients for energy conservation in the form of ATP4,5. The pathway is linear, not cyclic, it releases energy rather than requiring energy input, its enzymes are replete with primordial metal cofactors6,7, it traces to the last universal common ancestor8and abiotic, geochemical organic syntheses resembling segments of the pathway occur in hydrothermal vents today9,10. Laboratory simulations of the acetyl-CoA pathway’s reactions include the nonenzymatic synthesis of thioesters from CO and methylsulfide11, the synthesis of acetate12and pyruvate13from CO2using native iron or external electrochemical potentials14as the electron source. However, a full abiotic analogue of the acetyl-CoA pathway from H2and CO2as it occurs in life has not been reported to date. Here we show that three hydrothermal minerals — awaruite (Ni3Fe), magnetite (Fe3O4) and greigite (Fe3S4) — catalyse the fixation of CO2with H2at 100 °C under alkaline aqueous conditions. The product spectrum includes formate (100 mM), acetate (100 μM), pyruvate (10 μM), methanol (100 μM), and methane. With these simple catalysts, the overall exergonic reaction of the acetyl-CoA pathway is facile, shedding light on both the geochemical origin of microbial metabolism and on the nature of abiotic formate and methane synthesis in modern hydrothermal vents.

Rock–water–carbon interactions germane to serpentinization in hydrothermal vents have occurred for over 4 billion years, ever since there was liquid water on Earth. Serpentinization converts iron(II) containing minerals and water to magnetite (Fe3O4) plus H2. The hydrogen can generate native metals such as awaruite (Ni3Fe), a common serpentinization product. Awaruite catalyzes the synthesis of methane from H2 and CO2 under hydrothermal conditions. Native iron and nickel catalyze the synthesis of formate, methanol, acetate, and pyruvate—intermediates of the acetyl-CoA pathway, the most ancient pathway of CO2 fixation. Carbon monoxide dehydrogenase (CODH) is central to the pathway and employs Ni0 in its catalytic mechanism. CODH has been conserved during 4 billion years of evolution as a relic of the natural CO2-reducing catalyst at the onset of biochemistry. The carbide-containing active site of nitrogenase—the only enzyme on Earth that reduces N2—is probably also a relic, a biological reconstruction of the naturally occurring inorganic catalyst that generated primordial organic nitrogen. Serpentinization generates Fe3O4 and H2, the catalyst and reductant for industrial CO2 hydrogenation and for N2 reduction via the Haber–Bosch process. In both industrial processes, an Fe3O4 catalyst is matured via H2-dependent reduction to generate Fe5C2 and Fe2N respectively. Whether serpentinization entails similar catalyst maturation is not known. We suggest that at the onset of life, essential reactions leading to reduced carbon and reduced nitrogen occurred with catalysts that were synthesized during the serpentinization process, connecting the chemistry of life and Earth to industrial chemistry in unexpected ways.

Molecular hydrogen is an ancient source of energy and electrons. Anaerobic autotrophs that harness the H

Theories addressing the origin of life strive to explain the transition from rocks, water, inorganic carbon, and chondritic carbon (carbon from space) on the early Earth to living things (cells). The origin of life is generally regarded as the greatest of all evolutionary transitions and as one of the most difficult questions in all of the natural sciences. Energy, molecular organization, and the nature of the earliest life forms help to constrain the problem and link it to geochemical processes on the early Earth.

If life on Earth started out in geochemical environments like hydrothermal vents, then it started out from gasses like CO 2 , N 2 and H 2 . Anaerobic autotrophs still live from these gasses today, and they still inhabit the Earth's crust. In the search for connections between abiotic processes in ancient geological systems and biotic processes in biological systems, it becomes evident that chemical activation (catalysis) of these gasses and a constant source of energy are key. The H 2 –CO 2 redox reaction provides a constant source of energy and anabolic inputs, because the equilibrium lies on the side of reduced carbon compounds. Identifying geochemical catalysts that activate these gasses en route to nitrogenous organic compounds and small autocatalytic networks will be an important step towards understanding prebiotic chemistry that operates only on the basis of chemical energy, without input from solar radiation. So, if life arose in the dark depths of hydrothermal vents, then understanding reactions and catalysts that operate under such conditions is crucial for understanding origins.

All known life forms trace back to a last universal common ancestor (LUCA) that witnessed the onset of Darwinian evolution. One can ask questions about LUCA in various ways, the most common way being to look for traits that are common to all cells, like ribosomes or the genetic code. With the availability of genomes, we can, however, also ask what genes are ancient by virtue of their phylogeny rather than by virtue of being universal. That approach, undertaken recently, leads to a different view of LUCA than we have had in the past, one that fits well with the harsh geochemical setting of early Earth and resembles the biology of prokaryotes that today inhabit the Earth's crust.