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Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism

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Abstract

A minimal cell can be thought of as comprising informational, compartment-forming and metabolic subsystems. To imagine the abiotic assembly of such an overall system, however, places great demands on hypothetical prebiotic chemistry. The perceived differences and incompatibilities between these subsystems have led to the widely held assumption that one or other subsystem must have preceded the others. Here we experimentally investigate the validity of this assumption by examining the assembly of various biomolecular building blocks from prebiotically plausible intermediates and one-carbon feedstock molecules. We show that precursors of ribonucleotides, amino acids and lipids can all be derived by the reductive homologation of hydrogen cyanide and some of its derivatives, and thus that all the cellular subsystems could have arisen simultaneously through common chemistry. The key reaction steps are driven by ultraviolet light, use hydrogen sulfide as the reductant and can be accelerated by Cu(I)–Cu(II) photoredox cycling.

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Figure 1: Reaction network that leads to RNA, protein and lipid precursors.
Figure 2: Chemistry in a post-meteoritic-impact scenario.

References

  1. Gánti, T. The Principles of Life (Oxford Univ. Press, 2003).

    Book  Google Scholar 

  2. Dyson, F. Origins of Life 2nd edn (Cambridge Univ. Press, 1999).

    Book  Google Scholar 

  3. Orgel, L. E. Prebiotic chemistry and the origin of the RNA world. Crit. Rev. Biochem. Mol. Biol. 39, 99–123 (2004).

    CAS  Article  Google Scholar 

  4. Segré, D., Ben-Eli, D., Deamer, D. W. & Lancet, D. The lipid world. Orig. Life Evol. Biosph. 31, 119–145 (2001).

    Article  Google Scholar 

  5. Wächtershäuser, G. Groundworks for an evolutionary biochemistry: the iron–sulphur world. Prog. Biophys. Molec. Biol. 58, 85–201 (1992).

    Article  Google Scholar 

  6. Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).

    CAS  Article  Google Scholar 

  7. Mullen, L. B. & Sutherland, J. D. Simultaneous nucleotide activation and synthesis of amino acid amides by a potentially prebiotic multi-component reaction. Angew. Chem. Int. Ed. 46, 8063–8066 (2007).

    CAS  Article  Google Scholar 

  8. Ritson, D. & Sutherland, J. D. Prebiotic synthesis of simple sugars by photoredox systems chemistry. Nature Chem. 4, 895–899 (2012).

    CAS  Article  Google Scholar 

  9. Ritson, D. J. & Sutherland, J. D. Synthesis of aldehydic ribonucleotide and amino acid precursors by photoredox chemistry. Angew. Chem. Int. Ed. 52, 5845–5847 (2013).

    CAS  Article  Google Scholar 

  10. Yaylayan, V. A., Harty-Majors, S. & Ismail, A. A. Investigation of DL-glyceraldehyde-dihydroxyacetone interconversion by FTIR spectroscopy. Carbohydr. Res. 318, 20–25 (1999).

    CAS  Article  Google Scholar 

  11. Butzow, J. J. & Eichorn, G. L. Interactions of metal ions with polynucleotides and related compounds. IV. Degradation of polyribonucleotides by zinc and other divalent metal ions. Biopolymers 3, 95–107 (1965).

    CAS  Article  Google Scholar 

  12. Lombard, J., López-García, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nature Rev. Microbiol. 10, 507–515 (2012).

    CAS  Article  Google Scholar 

  13. Schlesinger, G. & Miller, S. L. Equilibrium and kinetics of glyconitrile formation in aqueous solution. J. Am. Chem. Soc. 95, 3729–3735 (1973).

    CAS  Article  Google Scholar 

  14. Kurosawa, K. et al. Hydrogen cyanide production due to mid-size impacts in a redox-neutral N2-rich atmosphere. Orig. Life Evol. Biosph. 43, 221–245 (2013).

    CAS  Article  Google Scholar 

  15. Pasek, M. A. & Lauretta, D. S. Aqueous corrosion of phosphide minerals from iron meteorites: a highly reactive source of prebiotic phosphorus on the surface of the early Earth. Astrobiology 5, 515–535 (2005).

    CAS  Article  Google Scholar 

  16. Bryant, D. E. & Kee, T. P. Direct evidence for the availability of reactive, water soluble phosphorus on the early Earth. H-Phosphinic acid from the Nantan meteorite. Chem. Commun. 2344–2346 (2006).

  17. Keefe, A. D. & Miller, S. L. Was ferrocyanide a prebiotic reagent? Orig. Life Evol. Biosph. 26, 111–129 (1996).

    CAS  Article  Google Scholar 

  18. Gáspár, V. & Beck, M. T. Kinetics of the photoaquation of hexacyanoferrate(II) ion. Polyhedron 2, 387–391 (1983).

    Article  Google Scholar 

  19. Rubin, A. E. Mineralogy of meteorite groups. Meteorit. Planet. Sci. 32, 231–247 (1997).

    CAS  Article  Google Scholar 

  20. Pincass, H. Die Bildung von Calciumcyanamid aus Ferrocyancalcium. Chem.-Ztg. 46, 661 (1922).

    CAS  Google Scholar 

  21. Seifer, G. B. The thermal decomposition of alkali cyanoferrates(II). Russ. J. Inorg. Chem. 7, 640–643 (1962).

    Google Scholar 

  22. Seifer, G. B. Thermal decomposition of alkaline earth metal and magnesium cyanoferrates(II). Russ. J. Inorg. Chem. 7, 1187–1189 (1962).

    Google Scholar 

  23. Yamanaka, M., Fujita, Y., McLean, A. & Iwase, M. A thermodynamic study of CaCN2 . High Temp. Mater. Processes 19, 275–279 (2000).

    CAS  Article  Google Scholar 

  24. Strecker, A. Ueber einen neuen aus Aldehyd-Ammoniak und Blausäure entstehenden Körper. Justus Liebigs Ann. Chem. 91, 349–351 (1854).

    Article  Google Scholar 

  25. Foster, G. W. A. The action of light on potassium ferrocyanide. J. Chem. Soc. 89, 912–920 (1906).

    CAS  Article  Google Scholar 

  26. Coderre, F. & Dixon, D. G. Modeling the cyanide heap leaching of cupriferous gold ores. Hydrometallurgy 52, 151–175 (1999).

    CAS  Article  Google Scholar 

  27. Hazen, R. M. Paleomineralogy of the Hadean eon: a preliminary species list. Am. J. Sci. 313, 807–843 (2013).

    CAS  Article  Google Scholar 

  28. Kurtz, P. Untersuchungen über die Bildung von Nitrilen. Liebigs Ann. Chem. 572, 23–82 (1951).

    CAS  Article  Google Scholar 

  29. Buc, S. R., Ford, J. H. & Wise, E. C. An improved synthesis of β-alanine. J. Am. Chem. Soc. 67, 92–94 (1945).

    CAS  Article  Google Scholar 

  30. Horváth, O. Photochemistry of copper(I) complexes. Coord. Chem. Rev. 135-136, 303–324 (1994).

    Article  Google Scholar 

  31. Baxendale, J. H. & Westcott, D. T. Kinetics and equilibria in copper(II)–cyanide solutions. J. Chem. Soc. 2347–2351 (1959).

  32. Moureu, C. & Bongrand, J-C. Le cyanoacetylene C3NH. Ann. Chim. (Paris) 14, 47–58 (1920).

    CAS  Google Scholar 

  33. Xiang, Y-B., Drenkard, S., Baumann, K., Hickey, D. & Eschenmoser, A. E. Chemie von α-Aminonitrilen. 12. Mitteilung. Sondierungen über thermische Umwandlungen von α-Aminonitrilen. Helv. Chim. Acta 77, 2209–2250 (1994).

    CAS  Article  Google Scholar 

  34. Miller, S. L. A production of amino acids under possible primitive Earth conditions. Science 117, 528–529 (1953).

    CAS  Article  Google Scholar 

  35. Butlerow, A. Bildung einer zuckerartigen Substanz durch Synthese. Liebigs Ann. Chem. 120, 295–298 (1861).

    Article  Google Scholar 

  36. Oró, J. Synthesis of adenine from ammonium cyanide. Biochem. Biophys. Res. Commun. 2, 407–412 (1960).

    Article  Google Scholar 

  37. Wegner, J., Ceylan, S. & Kirschning, A. Ten key issues in modern flow chemistry. Chem. Commun. 47, 4583–4592 (2011).

    CAS  Article  Google Scholar 

  38. de Duve, C. The onset of selection. Nature 433, 581–582 (2005).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

In memoriam Harry Lonsdale. This work was supported by the Medical Research Council (No. MC_UP_A024_1009), a grant from the Simons Foundation (No. 290362 to J.D.S.) and an award from the Origin of Life Challenge.

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J.D.S. supervised the research and the other authors performed the experiments. All the authors contributed intellectually as the project unfolded. J.D.S. wrote the paper and B.H.P. and C.P. assembled the Supplementary Information, additionally incorporating data from D.J.R. and C.D.D.

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Correspondence to John D. Sutherland.

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The authors declare no competing financial interests.

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Patel, B., Percivalle, C., Ritson, D. et al. Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nature Chem 7, 301–307 (2015). https://doi.org/10.1038/nchem.2202

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