Abstract
The transition from inorganic catalysis through minerals to organic catalysis by enzymes is a necessary step in the emergence of life. Our work is elucidating likely reactions at the earliest moments of Life, prior to the existence of enzymatic catalysis, by exploring essential intersections between nickel bioinorganic chemistry and pterin biochemistry. We used a prebiotically-inspired acetylene-containing volcanic hydrothermal experimental environment to shed light on the efficient formation of nickel-organo complexes. The simplest bis(dithiolene)nickel complex (C2H2S2)2Ni was identified by UV/Vis spectroscopy, mass spectrometry, nuclear magnetic resonance. Its temporal progression and possible function in this simulated early Earth atmosphere were investigated by isolating the main bis(dithiolene)nickel species from the primordial experimental setup. Using this approach, we uncovered a significant diversity of nickel-organo compositions by identifying 156 elemental annotations. The formation of acetaldehyde through the subsequent degradation of these organo-metal complexes is intriguing, as it is reminiscent of the ability of Pelobacter acetylenicus to hydrate acetylene to acetaldehyde via its bis(dithiolene)-containing enzyme acetylene hydratase. As our findings mechanistically characterize the role of nickel sulfide in catalyzing the formation of acetaldehyde, this fundamental pre-metabolic reaction could play the role of a primitive enzyme precursor of the enzymatic acetylene metabolism and further strengthen the role of acetylene in the molecular origin of life.
Similar content being viewed by others
Introduction
Initially, bis(dithiolene)nickel compounds garnered attention solely for their synthetic properties. However, their resemblance to enzyme catalytic centers was later recognized, leading to renewed attention for those nickel-organo compounds. The synthesis of thiophene from acetylene and pyrite (FeS2) by Steinkopf and Kirchhoff1 originally inspired Schrauzer and Mayweg to investigate the reactions between diphenyl acetylene and nickel sulfides in toluene2. Schrauzer’s discovery of bis(diphenyldithiolene)nickel, a nickel-sulfur complex with highly covalent metal-ligand bonds, led to the successful synthesis of various derivatives of this compound class, including the synthetically challenging unsubstituted complex (C2H2S2)2Ni, obtained from halogenated non-gaseous precursors and dissolved nickel ions3.
Several extant enzymes possess metal-dithiolene active cores binding to transition metals like tungsten or molybdenum4. One example is acetylene hydratase (AH) expressed by the anaerobic bacterium Pelobacter acetylenicus. This organism is frequently discussed in the context of the origin of life because of its unique ability to hydrate acetylene into acetaldehyde, leading to acetyl-CoA and acetate building blocks. Hyperthermophile Archaea thriving in the vicinity of volcanic hydrothermal vents express aldehyde ferredoxin oxidoreductase (AFO) with a tungstopterin center catalyzing the oxidation of aldehydes into carboxylic acids at 100 degrees Celsius (C°)4. Interestingly, the catalytic ability of enzymes relying on metal-dithiolenes can be enhanced by exchanging molybdenum with nickel in molybdopterin-like catalysts5. Regardless of the presence of an enzyme structure, the nickel bis(dithiolene) complex alone is an excellent electron transporter as it exists in three oxidation states (0, −1, −2). As a result, these complexes activate hydrogen more efficiently than most hydrogenases in Nature6, which aligns with the abiogenesis theory of prebiotic synthesis of organic molecules.
The role of acetylene as a building block of terrestrial life remains a topic of speculation. Still, there is growing evidence for its presence in the atmosphere of interstellar bodies such as Titan7 or Jupiter8. Additionally, its existence on early Earth is hypothesized9,10, emphasizing the importance of investigating the role of acetylene in the emergence of life. Previous hypotheses regarding the role of acetylene in the origin of life have suggested that it contributes to the formation of polycyclic aromatic hydrocarbons11 and small biomolecules12. Its popularity increased after it was proposed as a “fast food” for organisms in Earth’s early biosphere9. Recent literature analyzed the potential of acetylene under the same conditions to form distinct unsaturated fatty acids in combination with carbon monoxide13. Moreover, a route to pyrrole was demonstrated in the presence of ammonia, leading to the elemental unit of porphyrin, another metal complexing scaffold indispensable for life as we know it today. Acetylene, combined with nickel sulfide, forms a large diversity of prebiotic organic compounds, including acetaldehyde and alanine, in a one-pot setup14.
Nickel plays a fundamental role in enzymes found in most organisms, independent of the bis(dithiolene) framework. Nickel sites in extant enzymes show a large variety in nickel coordination and redox chemistry over a potential range of 1500 mV in proteins15. The metal center in superoxide dismutase (SOD) catalyzes redox processes with potentials ranging from +890–−160 mV16. In methyl-coenzyme M reductase (MCR) and carbon monoxide dehydrogenase (CODH), the active sites reach potentials as low as −600 mV17.
Anaerobic nickel-containing CODH isoforms are found in organisms capable of heterotrophy, autotrophy, fermentation, or anaerobic respiration18,19. In hydrogenogenic CO oxidizers, CO oxidation is coupled with proton reduction to produce hydrogen (H2)20. In the presence of water, required as an electron acceptor, a hydrogenase, and an ATP synthase are sufficient to ensure respiration. This straightforward mechanism highlights the significance of nickel-based catalysis in ancient energy preservation21.
Nickel sulfide plays a crucial role in recent prebiotic chemistry, as they were shown to promote multiple relevant reactions. Thioesters were synthesized on nickel sulfide through geoelectrochemical CO2 fixation22. Another study reported the promotion of a protometabolism in an alkaline hydrothermal vent environment23.“
Ni-organo catalysts are pivotal in various organic reactions, including cross-coupling reactions (e.g., Suzuki, Kumada, or Negishi couplings)24, carbon-heteroatom bond-forming25 reactions and the hydrogenation of organic compounds26. Our experimental setup finds its roots in the “Iron-sulfur world” theory of Wächtershäuser who considered nickel or iron sulfide salts as catalytically active species due to their redox potential and limited solubility in water, which allows surface catalysis.
We now further investigated the previously mentioned one-pot setup14 with a focus on the formation mechanism of acetaldehyde and its link to the presence of nickel-organo compounds. The one-pot setup already showed a progressing system that generated acetaldehyde over time and also changed its pH in the process due to formed acids, ultimately leading to a changed reaction path for the formed acetaldehyde. Building on the knowledge about the presence of acetaldehyde, we provide the first mechanistic evidence of abiogenic acetylene processing based on nickel bis(dithiolene), a molecular structure reminiscent of active centers of contemporary enzymes. Considering the resemblance with molybdopterin coenzymes, we postulate that nickel bis(dithiolene) was a transition catalyzer, allowing early acetaldehyde formation from acetylene in a prebiotic environment.
Results
Formation and identification of nickel-organo complexes
The investigated prebiotic system consisted of an oxygen-free carbon monoxide and acetylene atmosphere in equal amounts in the headspace of water containing water-insoluble nickel sulfide salt (NiS). The setup was contained in a sealed glass bottle and was incubated at 105 °C for varying periods of time.
The presence of nickel complexes was detected using Fourier-transform ion-cyclotron-resonance mass spectrometric (FT-ICR-MS) measurements after 2 h of incubation. FT-ICR-MS analysis allowed a reliable elemental annotation of the nickel-organo complexes in the complex reaction mixture. C4H4S4Ni was the most abundantly detected nickel-organo species by intensity. This annotation fits the simplest dithiolene-nickel species that can be obtained from two acetylene molecules, four sulfur, and one nickel atom. Due to its high abundance in the system, the composition could be further validated with its isotopic fine structure, excluding the possibility of false elemental annotation due to an isobaric compound (Fig. 1).
Samples showing the highest intensity of this compound in MS-spectra display a pink color (Suppl. Fig. 1). This color and the mass spectra signals for C4H4S4Ni decreased over time and were lost after 3 days of incubation.
A closer inspection of the isotope pattern revealed a further signal (Fig. 1, B+D highlighted in blue) not explained by the theoretical simulated isotope pattern. The mass difference between this additional peak and the isotope peak of the previous nominal mass amounts to the mass of one hydrogen atom. This result can be explained by the different possible oxidation states of nickel-bis(dithiolenes). The main peak belongs to the M-1 species. The additional peaks belong to the [X-2 + H+1]-1 species, with X being any isotopic species with a sufficiently high intensity to detect the second oxidation state species. The same observation was made for sodium ions but with lower signal intensity.
UV/VIS spectroscopy of the colored reaction product in water showed two absorption maxima at 500 and 855 nm. The second maximum is in the near-infrared at 855 nm. Absorption in the near-infrared is characteristic of bis(dithiolene)nickel compounds27. The maximum at 500 nm explained the observed pink color as absorption of green light results in red transmitted light and is also expected to be associated with the detected complex. Degradation of the complex in water happened relatively fast, and the corresponding UV/Vis signals nearly disappeared completely after 4 h at room temperature (Fig. 2, A). The degradation of the compound was accompanied by a color change of the solution from pink to yellow.
Isolation of the nickel-organo complex
We isolated the described complex from the aqueous solution via liquid-liquid extraction using methyl tert-butyl ether (MTBE). The MTBE phase took on a strongly violet color after the extraction of the aqueous phase. The MTBE phase was completely dried under N2 flow, and a dark blue solid remained in the glass vial. This color is also reported by Schrauzer, who synthesized the compound through a different non-aqueous route with halogenated reactants, incompatible with currently hypothesized conditions on early Earth3. We weighed the remaining solid of two different experimental setups in triplicates, differing in the composition of the gaseous atmosphere (Table 1). The setup with carbon monoxide produced 5.97 mg of the complex with a theoretical yield of 1.79%. In contrast, a setup with twice the volume of acetylene in the absence of carbon monoxide generated 6.92 mg with a yield of 1.14%. Utilizing twice the volume of acetylene increased the absolute yield as expected but decreased the theoretical yield. These yields are comparable to those reported by Schrauzer, who obtained a 3% yield using a more elaborate synthetic route. One triplicate of the CO/acetylene setup only showed very faint coloration. This triplicate also showed the lowest residual mass. A reaction scheme and discussed compounds can be found in the supplementary information (Suppl. Fig. 2).
The near insolubility of the isolated compound at room temperature in purified water strengthened our hypothesis of a changed charge state. Even though the color change could result purely from the solvent change, another explanation is the change of the complexes’ oxidation state from a charged water-soluble state to an uncharged lipophilic state. The solid only slowly dissolved at temperatures >50 °C, resulting in the expected pink coloration, followed by rapid degradation. Furthermore, adding the original reaction medium did not solubilize the compound at room temperature, excluding the possibility of a solubility-enhancing effect through molecules or salts formed in the experimental setup. Extraction of the residual solid phase in the reaction bottle with MTBE, expected to be mainly solid nickel sulfide salt, did not yield any amount of the target compound (no coloration of the MTBE used for extraction). We concluded that the compound remained solubilized during the experiment without precipitation and changed its oxidation state during extraction.
The isolated compound was further analyzed via LC-MS/MS to validate the hypothesized structure. LC-MS analysis of the dried extracted solid dissolved in methanol resulted in a violet solution with the same appearance as the MTBE solution. We detected the expected mass previously found in the initial mixture identified as (C2H2S2)2Ni-. Fragmentation was performed with a UHPLC-IM-Q-ToFMS system to gather fragmentation data (Fig. 2, B) and report its collision cross section (CCS) value of 130 Å2.
Fate of the formed nickel complex
The isolated water-insoluble complex became soluble at around 50 °C and above. Dissolution of the complex also resulted in a color change back to pink, comparable to the color of the unextracted aqueous mixture, reflecting the presence of the charged state in water.
Incubation of the isolated complex in water at pH 11 for 15 and 30 h resulted in the degradation of the complex. The degradation route and degradation products are temperature-dependent. The complex degraded into formic acid and acetaldehyde at temperatures reflecting the initial experimental conditions (100 °C) (Fig. 3). This result confirms the previously observed characteristics of those two compounds in the system and sheds light on the exact mechanism of their formation with nickel sulfide11. Incubation at 24 °C yielded no acetaldehyde. NMR measurements of the incubated sample showed increased signals in the olefinic ppm range. This observation shows the formation of new carbon-carbon bonds via this complex during its degradation. The complex degraded into unsaturated acetylene polymers. NMR spectra can be found in Supplementary data 1.
In the degradation process, nickel sulfide is consistently formed. The identification was made by observing an insoluble black solid in the reaction vessel. However, likely, the nickel and sulfur released during degradation precipitated at least partially into nickel sulfide. This particular process provides the complex with the ability to dissolve nickel sulfide, making it soluble, transport this highly insoluble salt and relocate it via diffusion processes.
Identification and characterization of diverse nickel-organo species
The compound with the elemental composition (C2H2S2)2Ni is not the only nickel-containing annotation in the mixture. 156 different elemental compositions were annotated, some containing various amounts of oxygen. The addition of oxygen to the sulfur atoms in those complexes was already described and discussed by Schrauzer28. The detected diversity of nickel-organo compounds is vast and sometimes challenging to interpret, as some elemental compositions contain odd amounts of carbon atoms, a fact hinting at a carbon cleavage pathway with nickel-organo compounds as intermediates. This hypothesis is also strengthened by the detection of formic acid after the degradation of the complex. Most annotations show the NiS4-core of the bis(dithiolene)nickel complex, followed in number by NiS3-“cores” (Fig. 4). It cannot be excluded that some or all NiS3-annotations result from in-source fragmentation, as the fragmentation pattern of [(C2H2S2)2Ni]- also showed a fragment with the formula [C2H2S3Ni]-. Nickel-organo annotations become increasingly scarce with higher amounts of sulfur atoms in the molecule. The NiS6-“core”-group is nearly devoid of signals. Only the [C6HxNiS6]- compositions (highlighted in yellow in Fig. 4) show some diversity in their homologous hydrogen series and could belong to the trimer, carrying an additional dithiolene unit.
Discussion
The formation of the reported bis(dithiolene) nickel complex after 2 h of incubation of the evolving reaction mixture showed the feasibility of its existence in early earth scenarios. The similarity of the formed bis(dithiolene) nickel complex with the active center of AH found in Pelobacter acetylenicus living in anaerobic aqueous systems is very intriguing, as the setting of the experiment is situated in a prebiotic oxygen-free atmosphere. Acetaldehyde is obtained from acetylene in the presence of NiS via the formed nickel bis(dithiolene) and then oxidized to acetic acid14(Fig. 5). This oxidation corresponds to a reaction performed by the hyperthermophilic archaeon Pyroccocus furiosus via AFO, another molybdopterin-containing enzyme. The likeness of the habitat of this microorganism is even more striking, as it lives near hydrothermal vents at 100 °C.
The described transportation role of the complex is also worth mentioning. The ability to extract nickel sulfide from minerals, to be later redeposited after degradation, leads to new scenarios, where nickel-catalyzed reactions like the reduction of double bonds29 can occur on primitive Earth. The change in polarity, from an ionic form into a highly lipophilic organic form, could also lead to enhanced complex uptake into vesicles with less permeable and hydrophobic properties. This aspect makes the reported complex not only relevant for early prebiotic stages but also for later stages during a transition from reactions in an aqueous bulk to an evolving metabolism in protocells. Its chemical nature facilitates its introduction into vesicular protocells. This hypothesis is strengthened by a recently published report of vesicle formation in the described set-up, where the formed long-chain fatty acids showed the potential to form vesicles30.
The described complexity of the nickel-organo complexes has the potential for the derivatization of this core motif for co-enzymes. Derivatization of the elemental nickel bis(dithiolene) alters its reactivity and potential to catalyze different reactions. The literature on nickel bis(dithiolene) complexes provides a large list of catalyzed reactions involved in the energy management of microorganisms. The reduction of hydrogen atoms to form hydrogen gas is among the most interesting. Bis(dithiolene) nickel complexes lower the reduction potential required for proton reduction resulting from formed acids6. Ameerunisha et al. reported the reduction of protons from p-toluene sulfonic acid through a nickel bis(dithiolene) complex6. The fact that this environment produced a large diversity of unsaturated carboxylic acids from carbon monoxide and acetylene13 increases the relevance of this mechanism, as those acids dissociate readily under aqueous conditions. The second origin of hydrogen cations in the system is acetic acid. Another reduction performed by those complexes is the reduction of CO2 into formic acid31. The ability of nickel bis(dithiolene) to act as an electron transporter and to exist in several oxidation states lets it perform energy transfer roles.
The formation of carboxylic acids synergizes well with the redox reactions catalyzed by this compound class. Metal-bis(dithiolene) compounds are potent hydrogenases. Nickel bis(dithiolene) complexes can reduce protons from organic acids to hydrogen gas6. One characteristic of the investigated system is the production of many highly unsaturated acids via Reppe chemistry13 and other acids. A compound reinforcing the suspected hydrogen activation is propanoic acid. Acrylic acid is the primary product of acetylene and carbon monoxide via the chemistry described by Reppe in 195332. Detection of its reduced form of propanoic acid33 in the mixture indirectly indicates a possible reduction with hydrogen gas.
In addition to its redox capabilities, bis(dithiolene) nickel compounds act as intermediates for many organo-sulfur compounds34. One main follow-up product of bis(dithiolene) nickel is thiophene, proven to exist in large amounts in the investigated mixture35.
Electron transfer is a vital mechanism of all living systems and is performed by NAD(H)/NADP(H) to allow ATP synthesis in extant organisms. The fact that acetylene is transformed to a large degree into aldehydes and additionally leads to a complex very similar to several active centers in enzymes connected to the metabolism of those compounds is a meaningful coincidence. A recent paper even showed its potential to oxidize glucose into gluconolactone36. Extant enzymes with pterin co-factors contain mostly molybdenum or tungsten. Yet nickel is a much more frequent element on Earth37 with an elemental abondance of 1.86% compared to Mo with 2.35 ppm and W with 180 ppb; therefore, the early existence of precursors of active centers with nickel is a plausible hypothesis. Additionally, nickel is found in the active centers of 9 contemporary enzymes (known so far)38. Further studies have to be performed to investigate what prebiotic conditions allow for an exchange of nickel through molybdenum or tungsten.”
Our findings revealed a pathway from acetylene to acetaldehyde via a nickel-organo complex. This discovery strengthens the relevance of nickel-organo compounds for the origin of life, as they now present an intermediate product for a prebiotic synthesis pathway of higher aldehydes, the amino acid alanine and potentially higher amino acids. Furthermore, this finding now paves the way for investigations about the exact catalytical nature and other roles in prebiotic chemistry of this nickel-organo compound.
Conclusion
This work showed the feasibility of forming bis(dithiolene) nickel under simulated early Earth atmosphere imitating hydrothermal volcanic conditions in the presence of acetylene. Even though the main nickel-organo compound (C2H2S2)2Ni is nearly water-insoluble, its spontaneous self-assembly from acetylene allows its charged existence in water. We characterized the structure of the detected nickel bis(dithiolene). We showed an intriguing similarity between the transformation of acetylene to acetaldehyde by the tungstopterin co-enzymes and the formation of acetaldehyde via the degradation of the self-assembled nickel bis(dithiolene). The structural resemblance between bis(dithiolene) and extant co-enzymes supports the hypothesis that metal bis(dithiolenes) may have been among the first protoenzymes. Altogether, our work explores an essential intersection between nickel bioinorganic chemistry and pterin biochemistry, elucidating likely reactions at the earliest moments prior to the existence of enzymatic catalysis.
Methods
Bottle setup
A 125 ml glass serum bottle was charged with 1.0 mmol NiSO4 • 6 H2O (99%, Aldrich) and sealed with a silicon stopper. The bottle underwent three cycles of evacuation and argon filling, ultimately reaching a deaerated state. Subsequently, the bottle was filled with argon-saturated water (calculated for the end volume of 5 ml), with 1.0 mL argon-saturated 1 M Na2S (solid Na2S: 99.99%, Aldrich) solution, with 1.0 mL 1 M NaOH solution and finally with 60 ml CO and 60 ml acetylene (acetone-free), using gastight syringes for the injections. Reactions were carried out at 105 °C. Following a reaction time of up to 3 days, the reaction mixture was cooled down.
FT-ICR-MS analysis
Samples were taken from the serum bottle with a syringe and centrifuged for 5 min at 15000 rpm. 100 µl of supernatant were diluted in 900 µl methanol and centrifuged to remove the precipitated salt. 70 µl of the centrifuged sample were diluted in 930 µl methanol to obtain the final sample dilution. Samples were measured in triplicates. All measurements were done in negative ionization mode.
Analysis was performed on a high-field Fourier Transform Ion Cyclotron Resonance mass spectrometer from Bruker Daltonics—Solarix. The magnet is a 12 T magnet from Magnex. The mass spectra were acquired with a 4 mega word (MW) time domain. The system was calibrated with L-arginine clusters in negative mode (5 mg L−1 L-arginine solved in methanol). For each sample, scans were accumulated in the mass range of 122–1000 amu. Ions were accumulated for 300 ms. The pressure in the hexapole was 3 × 10−6 mbar, and the pressure in the ICR vacuum chamber was 6 × 10−6 mbar. An Apollo ii (Bruker Daltonics) ESI source was used. The supernatant was injected via a microliter pump system (flow rate: 120 µl h−1).
Formula assignment was achieved through a network approach39.
LC-IM-Q-ToFMS analysis
LC-IM-MS/MS was carried out using a 6560 Ion Mobility LC/Q-TOF system (Agilent Technologies, Santa Clara, CA) coupled with a 1290 infinity II UHPLC (Agilent Technologies, Santa Clara, CA). Before the analysis, the MS was tuned within the parameters recommended by Agilent. The sample was injected onto a Waters ACQUITY UPLC BEH C8 (150 mm × 11 mm, 1.7 μm) column, with a starting gradient of 99% ACN (LC-MS/MS grade, Supelco LiChroSolv hypergrade for LC-MS) lowered linearly to 50% over 1 min with Milli-Q grade water and a total run time of 9 min at a flow rate of 0.2 mL/min. During the entire analysis, a reference mass mixture containing purine and hexakis(1H,1H,3H-tetrafluoropentoxy)phosphazene (Agilent Technologies, Santa Clara, CA) was introduced at a flow rate of 0.5 µL/min. The MS method used negative polarity with all ion fixed 2 ramped mode selected following drift time 0–59 with 10–40 CE in the second phase and a mass range from 50–1700. The gas temp was set at 250 °C with a flow of 12 L/min. The nebulizer was set at 40 psi, the sheath gas at 320 °C with a flow of 11 L/min, and vcap set at 5500 V. The IM measurements were conducted in N2 gas at ~4 Torr and 25 °C with a trap fill time of 2000 µs and release of 300 µs.
The raw file was calibrated to the reference mixture using an IM-MS reprocessor (Agilent Technologies, Santa Clara, CA), and the CCS was calibrated using a calibration mixture (Agilent Technologies, Santa Clara, CA) introduced to the IM-MS prior with a single field setting in Masshunter IM-MS browser (Agilent Technologies, Santa Clara, CA) result was applied to the sample measurement. Feature finding was carried out using an automatic and unbiased option in the mass profiler, and the CCS value resulted accordingly.
NMR analysis
D2O (for analysis, Merck KGaA) was prepared with added sodium trimethylsilylpropanoate (2 mM) (98 atom %D, Aldrich) as the internal standard. This solution was used to reference and quantify signals in 1D-1H experiments. The pH of the sodium phosphate buffer was adjusted to 11 with sodium hydroxide. This solution was used to keep the dissolved complex at pH 11. The buffer was deoxygenated by nitrogen purging.
Detection of degradation products
1D 1H spectra were acquired in triplicates for the dissolved complex in deoxygenated buffered water (100 mM sodium phosphate at pH11) after 0, 15, and 30 h of incubation at 100 °C. The sample at room temperature was prepared identically and measured after 30 h. 150 µl dissolved complex were spiked with 40 µl phosphate buffer and 10 µl D2O containing 2 mM TSP. The pulse program consisted of a simple 90° pulse followed by acquisition. 8 scans were acquired for each sample with a relaxation delay of 26 s and an acquisition time of 4 s. On-resonance pre-saturation was used during the relaxation delay to suppress the water signal. The optimized 90° pulse had a duration of 10.35 µs. Relative quantification was done by comparing the sum of the integrals after baseline correction of the hydrate single hydrogen signal and the methyl hydrogens signal to the TSP internal reference integral. The average for every time point was calculated. The acquired FID was apodized with an exponential function (LB = 0.3), and Fourier transformed.
Isolation of nickel bis(dithiolene)
We isolated the described complex from the aqueous solution via liquid-liquid extraction with methyl tert-butyl ether (MTBE). 9 mL of the reaction mixture was extracted with 3 × 9 mL of MTBE in a 50 ml falcon tube. The MTBE phase became strongly violet after the vortexing of the two-phase system. The MTBE phase was separated from the aqueous phase by carefully pipetting the MTBE off. The 3 × 9 ml of MTBE were combined and dried with an N2 flow. After reducing the volume to about 1 ml, the residual sample was transferred to a 1.5 ml glass vial that was weighed beforehand. The residual sample was then dried to completeness and weighed to determine the amount of solid in the glass vial. A dark blue solid remained in the glass vial. This procedure was repeated three times for the two examined gas ratios.
References
Steinkopf, W. & Kirchhoff, G. Studien in der thiophenreihe. I. die darstellung von thiophen aus acetylen. Justus Liebigs Ann. der Chem. 403, 1–11 (2006).
Schrauzer, G. N. & Mayweg, V. Reaction of diphenylacetylene with nickel sulfides. J. Am. Chem. Soc. 84, 3221–3221 (2002).
Schrauzer, G. N. & Mayweg, V. P. Coordination compounds with delocalized ground states, bisdithioglyoxalnickel and related complexes1a,b. J. Am. Chem. Soc. 87, 3585–3592 (2002).
Chan, M. K., Mukund, S., Kletzin, A., Adams, M. W. & Rees, D. C. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267, 1463–1469 (1995).
Fogeron, T. et al. A bioinspired nickel(bis-dithiolene) complex as a homogeneous catalyst for carbon dioxide electroreduction. ACS Catal. 8, 2030–2038 (2018).
Begum, A., Moula, G. & Sarkar, S. A nickel(II)-sulfur-based radical-ligand complex as a functional model of hydrogenase. Chemistry 16, 12324–12327 (2010).
Cable, M. L., Vu, T. H., Maynard-Casely, H. E., Choukroun, M. & Hodyss, R. The acetylene-ammonia co-crystal on titan. ACS Earth Space Chem. 2, 366–375 (2018).
Melin, H., Fletcher, L. N., Irwin, P. G. J. & Edgington, S. G. Jupiter in the ultraviolet: acetylene and ethane abundances in the stratosphere of Jupiter from Cassini observations between 0.15 and 0.19 μm. Astron. J. 159, 291 (2020).
Oremland, R. S. & Voytek, M. A. Acetylene as fast food: implications for development of life on anoxic primordial Earth and in the outer solar system. Astrobiology 8, 45–58 (2008).
Rimmer, P. B. & Shorttle, O. Origin of life’s building blocks in carbon and nitrogen-rich surface hydrothermal vents. Life (Basel) 9, 12 (2019).
Menor-Salvan, C., Ruiz-Bermejo, M., Osuna-Esteban, S., Munoz-Caro, G. & Veintemillas-Verdaguer, S. Synthesis of polycyclic aromatic hydrocarbons and acetylene polymers in ice: a prebiotic scenario. Chem. Biodivers. 5, 2729–2739 (2008).
Abbas O. & Schulze-Makuch D. Acetylene-based pathways for prebiotic evolution on titan. Exo-Astrobiology 518, 345–348 (2002).
Scheidler, C., Sobotta, J., Eisenreich, W., Wachtershauser, G. & Huber, C. Unsaturated C3,5,7,9-Monocarboxylic acids by aqueous, one-pot carbon fixation: possible relevance for the origin of life. Sci. Rep. 6, 27595 (2016).
Diederich, P. et al. Formation, stabilization and fate of acetaldehyde and higher aldehydes in an autonomously changing prebiotic system emerging from acetylene. Commun. Chem. 6, 38 (2023).
Ragsdale, S. W. Nickel-based enzyme systems. J. Biol. Chem. 284, 18571–18575 (2009).
Miller, A. F. Redox tuning over almost 1 V in a structurally conserved active site: lessons from Fe-containing superoxide dismutase. Acc. Chem. Res 41, 501–510 (2008).
Holliger, C., Pierik, A. J., Reijerse, E. J. & Hagen, W. R. A spectroelectrochemical study of factor F430 nickel(II/I) from methanogenic bacteria in aqueous solution. J. Am. Chem. Soc. 115, 5651–5656 (2002).
Inoue, M. et al. Structural and phylogenetic diversity of anaerobic carbon-monoxide dehydrogenases. Front Microbiol. 9, 3353 (2018).
Aragao, D., Mitchell, E. P., Frazao, C. F., Carrondo, M. A. & Lindley, P. F. Structural and functional relationships in the hybrid cluster protein family: structure of the anaerobically purified hybrid cluster protein from Desulfovibrio vulgaris at 1.35 A resolution. Acta Crystallogr D. Biol. Crystallogr 64, 665–674 (2008).
Fox, J. D., Kerby, R. L., Roberts, G. P. & Ludden, P. W. Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme. J. Bacteriol. 178, 1515–1524 (1996).
Schoelmerich, M. C. & Muller, V. Energy conservation by a hydrogenase-dependent chemiosmotic mechanism in an ancient metabolic pathway. Proc. Natl Acad. Sci. USA 116, 6329–6334 (2019).
Kitadai, N. et al. Thioester synthesis through geoelectrochemical CO(2) fixation on Ni sulfides. Commun. Chem. 4, 37 (2021).
Kitadai, N. et al. Metals likely promoted protometabolism in early ocean alkaline hydrothermal systems. Sci. Adv. 5, eaav7848 (2019).
Muto, K., Yamaguchi, J., Musaev, D. G. & Itami, K. Decarbonylative organoboron cross-coupling of esters by nickel catalysis. Nat. Commun. 6, 7508 (2015).
Hartwig, J. F. Carbon-heteroatom bond formation catalysed by organometallic complexes. Nature 455, 314–322 (2008).
Kamble, P. A., Vinod, C. P., Rathod, V. K. & Kantam, M. L. Hydrogenation of levulinic acid to gamma-valerolactone over nickel supported organoclay catalyst. Catal. Today 408, 36–49 (2023).
Miao, Q. et al. Syntheses and characterization of several nickel bis(dithiolene) complexes with strong and broad Near-IR absorption. Inorg. Chim. Acta. 376, 619–627 (2011).
Schrauzer, G. N., Zhang, C. & Chadha, R. The cis-bis(cis-2-mercaptostilbene-1-sulfinato)nickel(II) dianion: a product of the irreversible oxidation of the bis(cis-stilbene-1,2-dithiolato)nickel(II) dianion. Inorg. Chem. 29, 4104–4107 (2002).
Rauscher, S. A. & Moran, J. Hydrogen drives part of the reverse krebs cycle under metal or meteorite catalysis. Angew. Chem. Int Ed. Engl. 61, e202212932 (2022).
Geisberger, T. et al. Formation of vesicular structures from fatty acids formed under simulated volcanic hydrothermal conditions. Sci. Rep. 13, 15227 (2023).
Zhou, Y. et al. In(III) metal-organic framework incorporated with enzyme-mimicking Nickel Bis(dithiolene) ligand for highly selective CO(2) electroreduction. J. Am. Chem. Soc. 143, 14071–14076 (2021).
Reppe, W. Carbonylierung I. Über die umsetzung von acetylen mit kohlenoxyd und verbindungen mit reaktionsfähigen wasserstoffatomen synthesen α,β‐ungesättigter carbonsäuren und ihrer derivate. Justus Liebigs Ann. der Chem. 582, 1–37 (2006).
Sobotta, J. et al. A possible primordial acetyleno/carboxydotrophic core metabolism. Life (Basel) 10, 35 (2020).
Schrauzer, G. N. Coordination compounds with delocalized ground states, transition metal derivatives of dithiodiketones and ethylene-1,2-dithiolates (metal dithienes). Acc. Chem. Res. 2, 72–80 (2002).
Geisberger, T., Sobotta, J., Eisenreich, W. & Huber, C. Formation of thiophene under simulated volcanic hydrothermal conditions on earth-implications for early life on extraterrestrial planets. Life (Basel) 11, 149 (2021).
Zhou, Y. et al. A metal-organic framework based on a Nickel Bis(dithiolene) connector: synthesis, crystal structure and application as an electrochemical glucose sensor. J. Am. Chem. Soc. 142, 20313–20317 (2020).
Morgan, J. W. & Anders, E. Chemical composition of Earth, Venus, and Mercury. Proc. Natl Acad. Sci. USA 77, 6973–6977 (1980).
Alfano, M. & Cavazza, C. Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci. 29, 1071–1089 (2020).
Tziotis, D., Hertkorn, N. & Schmitt-Kopplin, P. Kendrick-analogous network visualisation of ion cyclotron resonance fourier transform mass spectra: improved options for the assignment of elemental compositions and the classification of organic molecular complexity. Eur. J. Mass Spectrom. (Chichester) 17, 415–421 (2011).
Acknowledgements
This research was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – Project-ID 364653263 – TRR 235 (CRC 235). CS and CH thank the Hans-Fischer-Gesellschaft (D-Munich) for financial support.
Funding
Open Access funding enabled and organized by Projekt DEAL.
Author information
Authors and Affiliations
Contributions
PD conceived and designed the analysis, collected the data, performed experiments, performed data analysis, and wrote the manuscript. CS, LB, LS, TG, and CH contributed analysis tools. TG and CS performed experiments. LB, LS, WE, CH, and PSK edited the manuscript. PSK, CH, and WE provided funding and supervised the project.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Communications Chemistry thanks all the anonymous reviewer for their contribution to the peer review of this work. A peer review file is available.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Diederich, P., Seitz, C., Buckett, L. et al. Nickel-organo compounds as potential enzyme precursors under simulated early Earth conditions. Commun Chem 7, 33 (2024). https://doi.org/10.1038/s42004-024-01119-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s42004-024-01119-0
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.