Extreme accumulation of ammonia on electroreduced mackinawite: An abiotic ammonia storage mechanism in early ocean hydrothermal systems.

An increasing amount of evidence suggests that early ocean hydrothermal systems were sustained sources of ammonia, an essential nitrogen species for prebiotic synthesis of life's building blocks. However, it remains a riddle how the abiotically generated ammonia was retained at the vent-ocean interface for the subsequent chemical evolution. Here, we demonstrate that, under simulated geoelectrochemical conditions in early ocean hydrothermal systems ([Formula: see text][Formula: see text] V versus the standard hydrogen electrode), mackinawite gradually reduces to zero-valent iron ([Formula: see text]), generating interlayer [Formula: see text] sites. This reductive conversion leads to an up to 55-fold increase in the solid/liquid partition coefficient for ammonia, enabling over 90% adsorption of 1 mM ammonia in 1 M NaCl at neutral pH. A coordinative binding of ammonia on the interlayer [Formula: see text] sites was computed to be the major mechanism of selective ammonia adsorption. Mackinawite is a ubiquitous sulfide precipitate in submarine hydrothermal systems. Given its reported catalytic function in amination, the extreme accumulation of ammonia on electroreduced mackinawite should have been a crucial initial step for prebiotic nitrogen assimilation, paving the way to the origin of life.

Amorphous Silica-Promoted Lysine Dimerization: a Thermodynamic Prediction.

It has long been suggested that mineral surfaces played a crucial role in the abiotic polymerization of amino acids that preceded the origin of life. Nevertheless, it remains unclear where the prebiotic process took place on the primitive Earth, because the amino acid-mineral interaction and its dependence on environmental conditions have yet to be understood adequately. Here we examined experimentally the adsorption of L-lysine (Lys) and its dimer (LysLys) on amorphous silica over a wide range of pH, ionic strength, adsorbate concentration, and the solid/water ratio, and determined the reaction stoichiometries and the equilibrium constants based on the extended triple-layer model (ETLM). The retrieved ETLM parameters were then used, in combination with the equilibrium constant for the peptide bond formation in bulk water, to calculate the Lys-LysLys equilibrium in the presence of amorphous silica under various aqueous conditions. Results showed that the silica surface favors Lys dimerization, and the influence varies greatly with changing environmental parameters. At slightly alkaline pH (pH 9) in the presence of a dilute NaCl (1 mM), the thermodynamically attainable LysLys from 0.1 mM Lys reached a concentration around 50 times larger than that calculated without silica. Because of the versatility of the ETLM, which has been applied to describe a wide variety of biomolecule-mineral interactions, future experiments with the reported methodology are expected to provide a significant constraint on the plausible geological settings for the condensation of monomers to polymers, and the subsequent chemical evolution of life.

Dissolved Divalent Metal and pH Effects on Amino Acid Polymerization: A Thermodynamic Evaluation.

Polymerization of amino acids is a fundamentally important step for the chemical evolution of life. Nevertheless, its response to changing environmental conditions has not yet been well understood because of the lack of reliable quantitative information. For thermodynamics, detailed prediction over diverse combinations of temperature and pH has been made only for a few amino acid-peptide systems. This study used recently reported thermodynamic dataset for the polymerization of the simplest amino acid "glycine (Gly)" to its short peptides (di-glycine and tri-glycine) to examine chemical and structural characteristics of amino acids and peptides that control the temperature and pH dependence of polymerization. Results showed that the dependency is strongly controlled by the intramolecular distance between the amino and carboxyl groups in an amino acid structure, although the side-chain group role is minor. The polymerization behavior of Gly reported earlier in the literature is therefore expected to be a typical feature for those of α-amino acids. Equilibrium calculations were conducted to examine effects of dissolved metals as a function of pH on the monomer-polymer equilibria of Gly. Results showed that metals shift the equilibria toward the monomer side, particularly at neutral and alkaline pH. Metals that form weak interaction with Gly (e.g., Mg2+) have no noticeable influence on the polymerization, although strong interaction engenders significant decrease of the equilibrium concentrations of Gly peptides. Considering chemical and structural characteristics of Gly and Gly peptides that control their interactions with metals, it can be expected that similar responses to the addition of metals are applicable in the polymerization of neutral α-amino acids. Neutral and alkaline aqueous environments with dissolved metals having high affinity with neutral α-amino acids (e.g., Cu2+) are therefore not beneficial places for peptide bond formation on the primitive Earth.

Glycine Polymerization on Oxide Minerals.

It has long been suggested that mineral surfaces played an important role in peptide bond formation on the primitive Earth. However, it remains unclear which mineral species was key to the prebiotic processes. This is because great discrepancies exist among the reported catalytic efficiencies of minerals for amino acid polymerizations, owing to mutually different experimental conditions. This study examined polymerization of glycine (Gly) on nine oxide minerals (amorphous silica, quartz, α-alumina and γ-alumina, anatase, rutile, hematite, magnetite, and forsterite) using identical preparation, heating, and analytical procedures. Results showed that a rutile surface is the most effective site for Gly polymerization in terms of both amounts and lengths of Gly polymers synthesized. The catalytic efficiency decreased as rutile > anatase > γ-alumina > forsterite > α- alumina > magnetite > hematite > quartz > amorphous silica. Based on reported molecular-level information for adsorption of Gly on these minerals, polymerization activation was inferred to have arisen from deprotonation of the NH3+ group of adsorbed Gly to the nucleophilic NH2 group, and from withdrawal of electron density from the carboxyl carbon to the surface metal ions. The orientation of adsorbed Gly on minerals is also a factor influencing the Gly reactivity. The examination of Gly-mineral interactions under identical experimental conditions has enabled the direct comparison of various minerals' catalytic efficiencies and has made discussion of polymerization mechanisms and their relative influences possible Further systematic investigations using the approach reported herein (which are expected to be fruitful) combined with future microscopic surface analyses will elucidate the role of minerals in the process of abiotic peptide bond formation.

Predicting Thermodynamic Behaviors of Non-Protein Amino Acids as a Function of Temperature and pH.

Why does life use α-amino acids exclusively as building blocks of proteins? To address that fundamental question from an energetic perspective, this study estimated the standard molal thermodynamic data for three non-α-amino acids (ß-alanine, γ-aminobutyric acid, and ε-aminocaproic acid) and α-amino-n-butyric acid in their zwitterionic, negative, and positive ionization states based on the corresponding experimental measurements reported in the literature. Temperature dependences of their heat capacities were described based on the revised Helgeson-Kirkham-Flowers (HKF) equations of state. The obtained dataset was then used to calculate the standard molal Gibbs energies (∆G (o)) of the non-α-amino acids as a function of temperature and pH. Comparison of their ∆G (o) values with those of α-amino acids having the same molecular formula showed that the non-α-amino acids have similar ∆G (o) values to the corresponding α-amino acids in physiologically relevant conditions (neutral pH, <100 °C). In acidic and alkaline pH, the non-α-amino acids are thermodynamically more stable than the corresponding α-ones over a broad temperature range. These results suggest that the energetic cost of synthesis is not an important selection pressure to incorporate α-amino acids into biological systems.

Energetics of Amino Acid Synthesis in Alkaline Hydrothermal Environments.

Alkaline hydrothermal systems have received considerable attention as candidates for the origin and evolution of life on the primitive Earth. Nevertheless, sufficient information has not yet been obtained for the thermodynamic properties of amino acids, which are necessary components for life, at high temperatures and alkaline pH. These properties were estimated using experimental high-temperature volume and heat capacity data reported in the literature for several amino acids, together with correlation algorithms and the revised Helgeson-Kirkham-Flowers (HKF) equations of state. This approach enabled determination of a complete set of the standard molal thermodynamic data and the revised HKF parameters for the 20 protein amino acids in their zwitterionic and ionization states. The obtained dataset was then used to evaluate the energetics of amino acid syntheses from simple inorganic precursors (CO2, H2, NH3 and H2S) in a simulated alkaline hydrothermal system on the Hadean Earth. Results show that mixing between CO2-rich seawater and the H2-rich hydrothermal fluid can produce energetically favorable conditions for amino acid syntheses, particularly in the lower-temperature region of such systems. Together with data related to the pH and temperature dependences of the energetics of amino acid polymerizations presented in earlier reports, these results suggest the following. Hadean alkaline hydrothermal settings, where steep pH and temperature gradients may have existed between cool, slightly acidic Hadean ocean water and hot, alkaline hydrothermal fluids at the vent-ocean interface, may be energetically the most suitable environment for the synthesis and polymerization of amino acids.

A Principled Approach to the Origin Problem.

The key issue of the origin of life is the origin of a complex system rather than the abiotic formation of various organic substances, small and large. To consider this "origin problem" it is advantageous to abstract some principles from biology and statistical physics to guide our approach. Referring to these principles, we aim to construct a chemical system called "protometabolism," which would be a precursor of metabolism.

Thermodynamic prediction of glycine polymerization as a function of temperature and pH consistent with experimentally obtained results.

Prediction of the thermodynamic behaviors of biomolecules at high temperature and pressure is fundamental to understanding the role of hydrothermal systems in the origin and evolution of life on the primitive Earth. However, available thermodynamic dataset for amino acids, essential components for life, cannot represent experimentally observed polymerization behaviors of amino acids accurately under hydrothermal conditions. This report presents the thermodynamic data and the revised HKF parameters for the simplest amino acid "Gly" and its polymers (GlyGly, GlyGlyGly and DKP) based on experimental thermodynamic data from the literature. Values for the ionization states of Gly (Gly(+) and Gly(-)) and Gly peptides (GlyGly(+), GlyGly(-), GlyGlyGly(+), and GlyGlyGly(-)) were also retrieved from reported experimental data by combining group additivity algorithms. The obtained dataset enables prediction of the polymerization behavior of Gly as a function of temperature and pH, consistent with experimentally obtained results in the literature. The revised thermodynamic data for zwitterionic Gly, GlyGly, and DKP were also used to estimate the energetics of amino acid polymerization into proteins. Results show that the Gibbs energy necessary to synthesize a mole of peptide bond is more than 10 kJ mol(-1) less than previously estimated over widely various temperatures (e.g., 28.3 kJ mol(-1) → 17.1 kJ mol(-1) at 25 °C and 1 bar). Protein synthesis under abiotic conditions might therefore be more feasible than earlier studies have shown.

Aqueous breakdown of aspartate and glutamate to n-ω-amino acids on the parent bodies of carbonaceous chondrites and asteroid Ryugu.

Amino acids in carbonaceous chondrites may have seeded the origin of life on Earth and possibly elsewhere. Recently, the return samples from a C-type asteroid Ryugu were found to contain amino acids with a similar distribution to Ivuna-type CI chondrites, suggesting the potential of amino acid abundances as molecular descriptors of parent body geochemistry. However, the chemical mechanisms responsible for the amino acid distributions remain to be elucidated particularly at low temperatures (<50°C). Here, we report that two representative proteinogenic amino acids, aspartic acid and glutamic acid, decompose to ß-alanine and γ-aminobutyric acid, respectively, under simulated geoelectrochemical conditions at 25°C. This low-temperature conversion provides a plausible explanation for the enrichment of these two n-ω-amino acids compared to their precursors in heavily aqueously altered CI chondrites and Ryugu's return samples. The results suggest that these heavily aqueously altered samples originated from the water-rich mantle of their water/rock differentiated parent planetesimals where protein α-amino acids were decomposed.

Photochemical Synthesis of Ammonia and Amino Acids from Nitrous Oxide.

Abiotic synthesis of ammonia (NH3) and amino acids is important for the origin of life and early evolution. Ammonia and organic nitrogen species may be produced from nitrous oxide (N2O), which is a second abundant nitrogen species in the atmosphere. Here, we report a new photochemical experiment and evaluate whether N2O can be used as a nitrogen source for prebiotic synthesis in the atmosphere. We conducted a series of experiments by using a gas mixture of N2O+CO, N2O+CO2, or N2O + H2 in the presence of liquid water. The results demonstrate that NH3, methylamine (CH3NH2), and some amino acids such as glycine, alanine, and serine can be synthesized through photochemistry from N2O even without metal catalysts. NH3 can be produced not only from CO + N2O, but also from H2+N2O. Glycine can be synthesized from CH3NH2 and CO2, which can be produced from N2O and CO under ultraviolet irradiation. Our work demonstrates, for the first time, that N2O could be an important nitrogen source and provide a new process for synthesizing ammonia and organic nitrogen species, which has not been previously considered. The contribution of organic synthesis from N2O should, therefore, be considered when discussing the prebiotic chemistry on primitive Earth.

Geoelectrochemistry-driven alteration of amino acids to derivative organics in carbonaceous chondrite parent bodies.

A long-standing question regarding carbonaceous chondrites (CCs) is how the CCs' organics were sourced and converted before and after the accretion of their parent bodies. Growing evidence shows that amino acid abundances in CCs decrease with an elongated aqueous alteration. However, the underlying chemical processes are unclear. If CCs' parent bodies were water-rock differentiated, pH and redox gradients can drive electrochemical reactions by using H2 as an electron source. Here, we simulate such redox conditions and demonstrate that α-amino acids are electrochemically altered to monoamines and α-hydroxy acids on FeS and NiS catalysts at 25 °C. This conversion is consistent with their enrichment compared to amino acid analogs in heavily altered CCs. Our results thus suggest that H2 can be an important driver for organic evolution in water-rock differentiated CC parent bodies as well as the Solar System icy bodies that might possess similar pH and redox gradients.

In situ FTIR study of CO2 reduction on inorganic analogues of carbon monoxide dehydrogenase.

The CO2-to-CO reduction by carbon monoxide dehydrogenase (CODH) with a [NiFe4S4] cluster is considered to be the oldest pathway of biological carbon fixation and therefore may have been involved in the origin of life. Although previous studies have investigated CO2 reduction by Fe and Ni sulfides to identify the prebiotic origin of the [NiFe4S4] cluster, the reaction mechanism remains largely elusive. Herein, we applied in situ electrochemical ATR-FTIR spectroscopy to probe the reaction intermediates of greigite (Fe3S4) and violarite (FeNi2S4). Intermediate species assignable to surface-bound CO2 and formyl groups were found to be stabilized in the presence of Ni, lending insight into its role in enhancing the multistep CO2 reduction process.

Electrochemically induced metal- vs. ligand-based redox changes in mackinawite: identification of a Fe3+- and polysulfide-containing intermediate.

Under anaerobic conditions, ferrous iron reacts with sulfide producing FeS, which can then undergo a temperature, redox potential, and pH dependent maturation process resulting in the formation of oxidized mineral phases, such as greigite or pyrite. A greater understanding of this maturation process holds promise for the development of iron-sulfide catalysts, which are known to promote diverse chemical reactions, such as H+, CO2 and NO3- reduction processes. Hampering the full realization of the catalytic potential of FeS, however, is an incomplete knowledge of the molecular and redox processess ocurring between mineral and nanoparticulate phases. Here, we investigated the chemical properties of iron-sulfide by cyclic voltammetry, Raman and X-ray absorption spectroscopic techniques. Tracing oxidative maturation pathways by varying electrode potential, nanoparticulate n(Fe2+S2-)(s) was found to oxidize to a Fe3+ containing FeS phase at -0.5 V vs. Ag/AgCl (pH = 7). In a subsequent oxidation, polysulfides are proposed to give a material that is composed of Fe2+, Fe3+, S2- and polysulfide (Sn2-) species, with its composition described as Fe2+1-3xFe3+2xS2-1-y(Sn2-)y. Thermodynamic properties of model compounds calculated by density functional theory indicate that ligand oxidation occurs in conjunction with structural rearrangements, whereas metal oxidation may occur prior to structural rearrangement. These findings together point to the existence of a metastable FeS phase located at the junction of a metal-based oxidation path between FeS and greigite (Fe2+Fe3+2S2-4) and a ligand-based oxidation path between FeS and pyrite (Fe2+(S2)2-).

Thioester synthesis through geoelectrochemical CO2 fixation on Ni sulfides.

A prevailing scenario of the origin of life postulates thioesters as key intermediates in protometabolism, but there is no experimental support for the prebiotic CO2 fixation routes to thioesters. Here we demonstrate that, under a simulated geoelectrochemical condition in primordial ocean hydrothermal systems (-0.6 to -1.0 V versus the standard hydrogen electrode), nickel sulfide (NiS) gradually reduces to Ni0, while accumulating surface-bound carbon monoxide (CO) due to CO2 electroreduction. The resultant partially reduced NiS realizes thioester (S-methyl thioacetate) formation from CO and methanethiol even at room temperature and neutral pH with the yield up to 35% based on CO. This thioester formation is not inhibited, or even improved, by 50:50 coprecipitation of NiS with FeS or CoS (the maximum yields; 27 or 56%, respectively). Such a simple thioester synthesis likely occurred in Hadean deep-sea vent environments, setting a stage for the autotrophic origin of life.

Thermodynamic Impact of Mineral Surfaces on Amino Acid Polymerization: Aspartate Dimerization on Goethite.

This article presents a thermodynamic predictive scheme for amino acid polymerization in the presence of minerals as a function of various environmental parameters (pH, ionic strength, amino acid concentration, and the solid/water ratio) using l-aspartate (Asp) and goethite as a model combination. This prediction is enabled by the combination of the surface adsorption constants of amino acid and its polymer, determined from the extended triple layer model characterization of the corresponding experimental results, with the thermodynamic data of these organic compounds in water reported in the literature. Calculations for the Asp-goethite system showed that the goethite surface drastically shifts the Asp monomer-dipeptide equilibrium toward the dipeptide side; when the dimerization of 0.1 mM Asp was considered in the presence of 10 m2 L-1 of goethite, an Asp dipeptide concentration around 105 times larger was computed to be thermodynamically attainable compared with that in the absence of goethite at acidic pH (4-5) and low ionic strength (0.1 mM NaCl). Under this condition, the dipeptide-to-monomer molecular ratio in the adsorbed state reached 20%. In contrast, no significant enhancement by goethite was predicted at alkaline pH (>8), where the electrostatic interactions of the goethite surface with Asp and Asp dipeptide are weak. Thus, mineral surfaces should have had a significant impact on the thermodynamics of prebiotic peptide bond formation on the early Earth, although the influences likely depended largely on the environmental conditions. Future experimental studies for various amino acid-mineral interactions using our proposed methodology will provide a quantitative constraint on favorable geochemical settings for the chemical evolution on Earth. This approach can also offer important clues for future exploration of extraterrestrial life.

Metals likely promoted protometabolism in early ocean alkaline hydrothermal systems.

One of the most plausible scenarios of the origin of life assumes the preceding prebiotic autotrophic metabolism in sulfide-rich hydrothermal vent environments. However, geochemical mechanisms to harness the reductive power provided by hydrothermal systems remain to be elucidated. Here, we show that, under a geoelectrochemical condition realizable in the early ocean hydrothermal systems, several metal sulfides (FeS, Ag2S, CuS, and PbS) undergo hour- to day-scale conversion to the corresponding metals at ≤-0.7 V (versus the standard hydrogen electrode). The electrochemically produced FeS-Fe0 assemblage promoted various reactions including certain steps in the reductive tricarboxylic acid cycle with efficiencies far superior to those due to pure FeS. The threshold potential is readily generated in the H2-rich alkaline hydrothermal systems that were probably ubiquitous on the Hadean seafloor. Thus, widespread metal production and metal-sustained primordial metabolism were likely to occur as a natural consequence of the active hydrothermal processes on the Hadean Earth.

Chemical Diversity of Metal Sulfide Minerals and Its Implications for the Origin of Life.

Prebiotic organic synthesis catalyzed by Earth-abundant metal sulfides is a key process for understanding the evolution of biochemistry from inorganic molecules, yet the catalytic functions of sulfides have remained poorly explored in the context of the origin of life. Past studies on prebiotic chemistry have mostly focused on a few types of metal sulfide catalysts, such as FeS or NiS, which form limited types of products with inferior activity and selectivity. To explore the potential of metal sulfides on catalyzing prebiotic chemical reactions, here, the chemical diversity (variations in chemical composition and phase structure) of 304 natural metal sulfide minerals in a mineralogy database was surveyed. Approaches to rationally predict the catalytic functions of metal sulfides are discussed based on advanced theories and analytical tools of electrocatalysis such as proton-coupled electron transfer, structural comparisons between enzymes and minerals, and in situ spectroscopy. To this end, we introduce a model of geoelectrochemistry driven prebiotic synthesis for chemical evolution, as it helps us to predict kinetics and selectivity of targeted prebiotic chemistry under "chemically messy conditions". We expect that combining the data-mining of mineral databases with experimental methods, theories, and machine-learning approaches developed in the field of electrocatalysis will facilitate the prediction and verification of catalytic performance under a wide range of pH and Eh conditions, and will aid in the rational screening of mineral catalysts involved in the origin of life.

Geochemistry and the Origin of Life: From Extraterrestrial Processes, Chemical Evolution on Earth, Fossilized Life's Records, to Natures of the Extant Life.

In 2001, the first author (S.N.) led the publication of a book entitled "Geochemistry and the origin of life" in collaboration with Dr. Andre Brack aiming to figure out geo- and astro-chemical processes essential for the emergence of life. Since then, a great number of research progress has been achieved in the relevant topics from our group and others, ranging from the extraterrestrial inputs of life's building blocks, the chemical evolution on Earth with the aid of mineral catalysts, to the fossilized records of ancient microorganisms. Here, in addition to summarizing these findings for the origin and early evolution of life, we propose a new hypothesis for the generation and co-evolution of photosynthesis with the redox and photochemical conditions on the Earth's surface. Besides these bottom-up approaches, we introduce an experimental study on the role of water molecules in the life's function, focusing on the transition from live, dormant, and dead states through dehydration/hydration. Further spectroscopic studies on the hydrogen bonding behaviors of water molecules in living cells will provide important clues to solve the complex nature of life.

Geoelectrochemical CO production: Implications for the autotrophic origin of life.

Wächtershäuser's proposal of the autotrophic origin of life theory and subsequent laboratory demonstrations of relevant organic reactions have opened a new gate for the exploration of the origin of life. However, this scenario remains controversial because, at present, it requires a high pressure of CO as a source of carbon and reducing energy, although CO must have been a trace C species on the Hadean Earth. We show that, simulating a geoelectrochemical environment in deep-sea hydrothermal fields, CO production with up to ~40% Faraday efficiency was attainable on CdS in CO2-saturated NaCl solution at ≤-1 V (versus the standard hydrogen electrode). The threshold potential is readily generated in the H2-rich, high-temperature, and alkaline hydrothermal vents that were probably widespread on the early komatiitic and basaltic ocean crust. Thus, Wächtershäuser's scenario starting from CO2 was likely to be realized in the Hadean ocean hydrothermal systems.