Nickel-organo compounds as potential enzyme precursors under simulated early Earth conditions.


Journal

Communications chemistry
ISSN: 2399-3669
Titre abrégé: Commun Chem
Pays: England
ID NLM: 101725670

Informations de publication

Date de publication:
15 Feb 2024
Historique:
received: 21 10 2023
accepted: 01 02 2024
medline: 16 2 2024
pubmed: 16 2 2024
entrez: 16 2 2024
Statut: epublish

Résumé

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 (C

Identifiants

pubmed: 38361005
doi: 10.1038/s42004-024-01119-0
pii: 10.1038/s42004-024-01119-0
doi:

Types de publication

Journal Article

Langues

eng

Pagination

33

Informations de copyright

© 2024. The Author(s).

Références

Steinkopf, W. & Kirchhoff, G. Studien in der thiophenreihe. I. die darstellung von thiophen aus acetylen. Justus Liebigs Ann. der Chem. 403, 1–11 (2006).
doi: 10.1002/jlac.19144030102
Schrauzer, G. N. & Mayweg, V. Reaction of diphenylacetylene with nickel sulfides. J. Am. Chem. Soc. 84, 3221–3221 (2002).
doi: 10.1021/ja00875a061
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).
doi: 10.1021/ja01094a011
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).
doi: 10.1126/science.7878465 pubmed: 7878465
Fogeron, T. et al. A bioinspired nickel(bis-dithiolene) complex as a homogeneous catalyst for carbon dioxide electroreduction. ACS Catal. 8, 2030–2038 (2018).
doi: 10.1021/acscatal.7b03383
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).
doi: 10.1002/chem.201001812 pubmed: 20853299
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).
doi: 10.1021/acsearthspacechem.7b00135
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).
doi: 10.3847/1538-3881/ab91a6
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).
doi: 10.1089/ast.2007.0183 pubmed: 18199006
Rimmer, P. B. & Shorttle, O. Origin of life’s building blocks in carbon and nitrogen-rich surface hydrothermal vents. Life (Basel) 9, 12 (2019).
pubmed: 30682803
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).
doi: 10.1002/cbdv.200890228 pubmed: 19089832
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).
doi: 10.1038/srep27595 pubmed: 27283227 pmcid: 4901337
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).
doi: 10.1038/s42004-023-00833-5 pubmed: 36813975 pmcid: 9947100
Ragsdale, S. W. Nickel-based enzyme systems. J. Biol. Chem. 284, 18571–18575 (2009).
doi: 10.1074/jbc.R900020200 pubmed: 19363030 pmcid: 2707248
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).
doi: 10.1021/ar700237u pubmed: 18376853
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).
doi: 10.1021/ja00066a034
Inoue, M. et al. Structural and phylogenetic diversity of anaerobic carbon-monoxide dehydrogenases. Front Microbiol. 9, 3353 (2018).
doi: 10.3389/fmicb.2018.03353 pubmed: 30705673
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).
doi: 10.1107/S0907444908009165 pubmed: 18560155
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).
doi: 10.1128/jb.178.6.1515-1524.1996 pubmed: 8626276 pmcid: 177833
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).
doi: 10.1073/pnas.1818580116 pubmed: 30850546 pmcid: 6442639
Kitadai, N. et al. Thioester synthesis through geoelectrochemical CO(2) fixation on Ni sulfides. Commun. Chem. 4, 37 (2021).
doi: 10.1038/s42004-021-00475-5 pubmed: 36697522 pmcid: 9814748
Kitadai, N. et al. Metals likely promoted protometabolism in early ocean alkaline hydrothermal systems. Sci. Adv. 5, eaav7848 (2019).
doi: 10.1126/sciadv.aav7848 pubmed: 31223650 pmcid: 6584212
Muto, K., Yamaguchi, J., Musaev, D. G. & Itami, K. Decarbonylative organoboron cross-coupling of esters by nickel catalysis. Nat. Commun. 6, 7508 (2015).
doi: 10.1038/ncomms8508 pubmed: 26118733
Hartwig, J. F. Carbon-heteroatom bond formation catalysed by organometallic complexes. Nature 455, 314–322 (2008).
doi: 10.1038/nature07369 pubmed: 18800130 pmcid: 2819340
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).
doi: 10.1016/j.cattod.2022.10.004
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).
doi: 10.1016/j.ica.2011.07.046
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).
doi: 10.1021/ic00345a039
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).
doi: 10.1002/anie.202212932 pubmed: 36251920 pmcid: 10100321
Geisberger, T. et al. Formation of vesicular structures from fatty acids formed under simulated volcanic hydrothermal conditions. Sci. Rep. 13, 15227 (2023).
doi: 10.1038/s41598-023-42552-w pubmed: 37710028 pmcid: 10502091
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).
doi: 10.1021/jacs.1c06797 pubmed: 34450022
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).
doi: 10.1002/jlac.19535820102
Sobotta, J. et al. A possible primordial acetyleno/carboxydotrophic core metabolism. Life (Basel) 10, 35 (2020).
pubmed: 32272667
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).
doi: 10.1021/ar50015a002
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).
pubmed: 33669362
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).
doi: 10.1021/jacs.0c09009
Morgan, J. W. & Anders, E. Chemical composition of Earth, Venus, and Mercury. Proc. Natl Acad. Sci. USA 77, 6973–6977 (1980).
doi: 10.1073/pnas.77.12.6973 pubmed: 16592930 pmcid: 350422
Alfano, M. & Cavazza, C. Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci. 29, 1071–1089 (2020).
doi: 10.1002/pro.3836 pubmed: 32022353 pmcid: 7184782
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).
doi: 10.1255/ejms.1135 pubmed: 22006638

Auteurs

Philippe Diederich (P)

Helmholtz Munich, Research Unit Analytical BioGeoChemistry, Neuherberg, Germany.

Christian Seitz (C)

Technical University of Munich, TUM School of Natural Sciences, Department of Bioscience, Bavarian NMR Center (BNMRZ), Structural Membrane Biochemistry, Lichtenbergstr. 4, 85748, Garching, Germany.

Lance Buckett (L)

Helmholtz Munich, Research Unit Analytical BioGeoChemistry, Neuherberg, Germany.

Liesa Salzer (L)

Helmholtz Munich, Research Unit Analytical BioGeoChemistry, Neuherberg, Germany.

Thomas Geisberger (T)

Technical University of Munich, TUM School of Natural Sciences, Department of Bioscience, Bavarian NMR Center (BNMRZ), Structural Membrane Biochemistry, Lichtenbergstr. 4, 85748, Garching, Germany.

Wolfgang Eisenreich (W)

Technical University of Munich, TUM School of Natural Sciences, Department of Bioscience, Bavarian NMR Center (BNMRZ), Structural Membrane Biochemistry, Lichtenbergstr. 4, 85748, Garching, Germany.

Claudia Huber (C)

Technical University of Munich, TUM School of Natural Sciences, Department of Bioscience, Bavarian NMR Center (BNMRZ), Structural Membrane Biochemistry, Lichtenbergstr. 4, 85748, Garching, Germany.

Philippe Schmitt-Kopplin (P)

Helmholtz Munich, Research Unit Analytical BioGeoChemistry, Neuherberg, Germany. schmitt-kopplin@helmholtz-muenchen.de.
Comprehensive Foodomics Platform, Chair of Analytical Food Chemistry, TUM School of Life Sciences, Technical University of Munich, Maximus-von-Imhof-Forum 2, 85354, Freising, Germany. schmitt-kopplin@helmholtz-muenchen.de.
Max Planck Institute for Extraterrestrial Physics, Center for Astrochemical Studies, Gießebachstraße 1, 85748, Garching bei München, Germany. schmitt-kopplin@helmholtz-muenchen.de.

Classifications MeSH