Energy at Origins: Favorable Thermodynamics of Biosynthetic Reactions in the Last Universal Common Ancestor (LUCA)

Though all theories for the origin of life require a source of energy to promote primordial chemical reactions, the nature of energy that drove the emergence of metabolism at origins is still debated. We reasoned that evidence for the nature of energy at origins should be preserved in the biochemical reactions of life itself, whereby changes in free energy, ΔG, which determine whether a reaction can go forward or not, should help specify the source. By calculating values of ΔG across the conserved and universal core of 402 individual reactions that synthesize amino acids, nucleotides and cofactors from H2, CO2, NH3, H2S and phosphate in modern cells, we find that 95-97% of these reactions are exergonic (ΔG ≤ 0 kJ⋅mol-1) at pH 7-10 and 80-100°C under nonequilibrium conditions with H2 replacing biochemical reductants. While 23% of the core's reactions involve ATP hydrolysis, 77% are ATP-independent, thermodynamically driven by ΔG of reactions involving carbon bonds. We identified 174 reactions that are exergonic by -20 to -300 kJ⋅mol-1 at pH 9 and 80°C and that fall into ten reaction types: six pterin dependent alkyl or acyl transfers, ten S-adenosylmethionine dependent alkyl transfers, four acyl phosphate hydrolyses, 14 thioester hydrolyses, 30 decarboxylations, 35 ring closure reactions, 31 aromatic ring formations, and 44 carbon reductions by reduced nicotinamide, flavins, ferredoxin, or formate. The 402 reactions of the biosynthetic core trace to the last universal common ancestor (LUCA), and reveal that synthesis of LUCA's chemical constituents required no external energy inputs such as electric discharge, UV-light or phosphide minerals. The biosynthetic reactions of LUCA uncover a natural thermodynamic tendency of metabolism to unfold from energy released by reactions of H2, CO2, NH3, H2S, and phosphate

Serpentinization: Connecting geochemistry, ancient metabolism and industrial hydrogenation

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

A hydrogen-dependent geochemical analogue of primordial carbon and energy metabolism

Hydrogen gas, H2, is generated by alkaline hydrothermal vents through an ancient geochemical process called serpentinization in which water reacts with iron containing minerals deep within the Earth's crust. H2 is the electron donor for the most ancient and the only energy releasing route of biological CO2 fixation, the acetyl-CoA pathway. At the origin of metabolism, CO2 fixation by hydrothermal H2 within serpentinizing systems could have preceded and patterned biotic pathways. Here we show that three hydrothermal minerals—greigite (Fe3S4), magnetite (Fe3O4) and awaruite (Ni3Fe)—catalyse the fixation of CO2 with H2 at 100°C under alkaline aqueous conditions. The product spectrum includes formate (up to 200 mM), acetate (up to 100 µM), pyruvate (up to 10 µM), methanol (up to 100 µM), and methane. The results shed light on both the geochemical origin of microbial metabolism and on the nature of abiotic formate and methane synthesis in modern hydrothermal vents

INTERACTION OF TORSION AND OVERALL ROTATION IN P-CRESOL

$^{1}$ M. Gerhards, B. Kimpfel, M. Pohl, M. Schmitt, K. Kleinermanns J. Mol. Struct. 270. 301 (1992)Author Institution: Institut f\""{u}r physikalische Chemie, Heinriche Heine Universit\""{a}tThe 1e-2e torsional band of the near prolate asymmetric rotor p-cresol shows a significantly broadened structure in comparison to the electronic origin 0a1-0a1. This broadening is due to an interaction between the torsional vibration of the methylgroup and the overall rotation of the molecule, which is absent in the case of the electronic $origin^{1}$. This interaction is strong, because the axis of internal rotation (z) and overall rotation (a) nearly coincide in the case of p-cresol. A simulation of the rotational band contour of the le-2e band, including this interaction leads to the following rotational constants [$cm^{-1}$]: $\begin{array}{lll}A^{\prime \prime}= 0.183603& B^{\prime \prime}= 0.048573& C^{\prime \prime}= 0.038685\\ A^{\prime} = 0.172803& B^{\prime} = 0.049173& C^{\prime} = 0.038525\end{array}$ Within the error these are the same rotational constants as obtained by simulation of the electronic origin Oai-Oai of p-cresol. A simulation of the le-2e band without consideration of the perturbation is only succesfull under the assumption of a very large change of the rotational constant A, which has no physical meaning

SPECTRAL HOLE BURNING AS PROBE OF INTERMOLECULAR VIBRATIONS IN HYDROGEN BONDED MOLECULAR COMPLEXES

[1] S.A. Wittmeyer, M.R. Topp, Chem. Phys. Lett. 163, 261 (1989) [2] M. Schmitt, H. M\""{u}ller, K. Kleinermanns, Chem. Phys. Lett. accepted for publication (1994)Author Institution: Institut for physikalische Chemie I, Heinrich-Heine-Universit\""{a}t D\""{u}sseldorf UniversitatsstrSeveral hydrogen bonded clusters of phenol with water, methanol and phenol were examined by spectral hole burning (SHB). The ground state is depopulated persistently on the time scale of the experiment by a tunable dye laser (burn laser). After a variable time delay (400 to 800 ns) the population of the ground state level is probed by a second dye laser. If probe and burn laser share a common ground state level, the fluorescence caused by the probe later is decreased [1]. Because of cluster and state selectivity of spectral hole burning, several intermolecular vibrations of Phenol. $(H_{2}O)_{3}$ could be assigned for the first time[2]. In opposite to Resonance Enhanced multiphoton Ionisation with time flight detection (REMPI-TOF) fragmentation of the clusters does not perturb the spectrum Different conformers of one cluster size can be distinguished by SHB. The phenol dimer provides an interesting example of a cluster with tow closely neighbouring elcectronically excited states. These excited states belong to the donor and the acceptor chromophore respectively. Spectral hole burning provides new insights in the vibrational structure of this cluster and in dynamic process between the different potential surfaces