Nature

A prebiotically plausible scenario of an RNA–peptide world

  • Gilbert, W. Origin of life: the RNA world. Nature 319, 618 (1986).

    Article 
    ADS 

    Google Scholar
     

  • Orgel, L. E. Evolution of the genetic apparatus. J. Mol. Biol. 38, 381–393 (1968).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Crick, F. H. C., Brenner, S., Klug, A. & Pieczenik, G. A speculation on the origin of protein synthesis. Orig. Life Evol. Biosph. 7, 389–397 (1976).

    CAS 
    Article 

    Google Scholar
     

  • Joyce, G. F. The antiquity of RNA-based evolution. Nature 418, 214–221 (2002).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Bowman, J. C., Hud, N. V. & Williams, L. D. The ribosome challenge to the RNA world. J. Mol. Evol. 80, 143–161 (2015).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Decatur, W. A. & Fournier, M. J. rRNA modifications and ribosome function. Trends Biochem. Sci 27, 344–351 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Carell, T. et al. Structure and function of noncanonical nucleobases. Angew. Chem. Int. Ed. Engl. 51, 7110–7131 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Wong, J. T.-F. Origin of genetically encoded protein synthesis: a model based on selection for RNA peptidation. Orig. Life Evol. Biosph. 21, 165–176 (1991).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Di Giulio, M. Reflections on the origin of the genetic code: a hypothesis. J. Theor. Biol. 191, 191–196 (1998).

    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Rios, A. C. & Tor, Y. On the origin of the canonical nucleobases: an assessment of selection pressures across chemical and early biological evolution. Isr. J. Chem. 53, 469–483 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Grosjean, H. & Westhof, E. An integrated, structure- and energy-based view of the genetic code. Nucleic Acids Res. 44, 8020–8040 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Beenstock, J. & Sicheri, F. The structural and functional workings of KEOPS. Nucleic Acids Res. 49, 10818–10834 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Di Giulio, M. On the RNA world: evidence in favor of an early ribonucleopeptide world. J. Mol. Evol. 45, 571–578 (1997).

    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Ramakrishnan, V. Ribosome structure and the mechanism of translation. Cell 108, 557–572 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Fox, G. E. Origin and evolution of the ribosome. Cold Spring Harb. Perspect. Biol. 2, a003483 (2010).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bowman, J. C., Petrov, A. S., Frenkel-Pinter, M., Penev, P. I. & Williams, L. D. Root of the tree: the significance, evolution, and origins of the ribosome. Chem. Rev. 120, 4848–4878 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Eigen, M. & Schuster, P. A principle of natural self-organization. Naturwissenschaften 64, 541–565 (1977).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Szathmáry, E. Coding coenzyme handles: a hypothesis for the origin of the genetic code. Proc. Natl Acad. Sci. USA 90, 9916–9920 (1993).

    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar
     

  • Noller, H. F. RNA structure: reading the ribosome. Science 309, 1508–1514 (2005).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Steitz, T. A. A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 9, 242–253 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat. Rev. Microbiol. 1, 127–136 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Woese, C. The universal ancestor. Proc. Natl Acad. Sci. USA 95, 6854–6859 (1998).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar
     

  • Becerra, A., Delaye, L., Islas, S. & Lazcano, A. The very early stages of biological evolution and the nature of the last common ancestor of the three major cell domains. Annu. Rev. Ecol. Evol. Syst. 38, 361–379 (2007).

    Article 

    Google Scholar
     

  • Kuhn, H. Self-organization of molecular systems and evolution of the genetic apparatus. Angew. Chem. Int. Ed. Engl. 11, 798–820 (1972).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Kuhn, H. & Waser, J. Molecular self-organization and the origin of life. Angew. Chem. Int. Ed. Engl. 20, 500–520 (1981).

    Article 

    Google Scholar
     

  • Tamura, K. & Schimmel, P. Oligonucleotide-directed peptide synthesis in a ribosome- and ribozyme-free system. Proc. Natl Acad. Sci. USA 98, 1393–1397 (2001).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar
     

  • Tamura, K. & Schimmel, P. Peptide synthesis with a template-like RNA guide and aminoacyl phosphate adaptors. Proc. Natl Acad. Sci. USA 100, 8666–8669 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar
     

  • Turk, R. M., Chumachenko, N. V. & Yarus, M. Multiple translational products from a five-nucleotide ribozyme. Proc. Natl Acad. Sci. USA 107, 4585–4589 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar
     

  • Jash, B., Tremmel, P., Jovanovic, D. & Richert, C. Single nucleotide translation without ribosomes. Nat. Chem. 13, 751–757 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Forsythe, J. G. et al. Ester-mediated amide bond formation driven by wet–dry cycles: a possible path to polypeptides on the prebiotic Earth. Angew. Chem. Int. Ed. Engl. 54, 9871–9875 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Becker, S. et al. Wet-dry cycles enable the parallel origin of canonical and non-canonical nucleosides by continuous synthesis. Nat. Commun. 9, 163 (2018).

    PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Tetzlaff, C. N. & Richert, C. Synthesis and hydrolytic stability of 5′-aminoacylated oligouridylic acids. Tetrahedron Lett. 42, 5681–5684 (2001).

    CAS 
    Article 

    Google Scholar
     

  • Schweizer, M. P., McGrath, K. & Baczynskyj, L. The isolation and characterization of N-[9-(βd-ribofuranosyl)-purin-6-ylcarbamoyl]glycine from yeast transfer RNA. Biochem. Biophys. Res. Commun. 40, 1046–1052 (1970).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Perrochia, L. et al. In vitro biosynthesis of a universal t6A tRNA modification in Archaea and Eukarya. Nucleic Acids Res. 41, 1953–1964 (2012).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • Kimura-Harada, F., Von Minden, D. L., McCloskey, J. A. & Nishimura, S. N-[(9-βd-Ribofuranosylpurin-6-yl)-N-methylcarbamoyl]threonine, a modified nucleoside isolated from Escherichia coli threonine transfer ribonucleic acid. Biochemistry 11, 3910–3915 (1972).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Robertson, M. & Miller, S. Prebiotic synthesis of 5-substituted uracils: a bridge between the RNA world and the DNA-protein world. Science 268, 702–705 (1995).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Murphy, F. V., Ramakrishnan, V., Malkiewicz, A. & Agris, P. F. The role of modifications in codon discrimination by tRNALysUUU. Nat. Struct. Mol. Biol. 11, 1186–1191 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Kitamura, A. et al. Characterization and structure of the Aquifex aeolicus protein DUF752: a bacterial tRNA-methyltransferase (MnmC2) functioning without the usually fused oxidase domain (MnmC1). J. Biol. Chem. 287, 43950–43960 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Hutchby, M. et al. Hindered ureas as masked isocyanates: facile carbamoylation of nucleophiles under neutral conditions. Angew. Chem. Int. Ed. Engl. 48, 8721–8724 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Ohkubo, A. et al. New thermolytic carbamoyl groups for the protection of nucleobases. Org. Biomol. Chem. 7, 687–694 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Nainytė, M. et al. Amino acid modified RNA bases as building blocks of an early Earth RNA-peptide world. Chem. Eur. J. 26, 14856–14860 (2020).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • Schimpl, A., Lemmon, R. M. & Calvin, M. Cyanamide formation under primitive Earth conditions. Science 147, 149–150 (1965).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Gartner, Z. J., Kanan, M. W. & Liu, D. R. Expanding the reaction scope of DNA-templated synthesis. Angew. Chem. Int. Ed. Engl. 41, 1796–1800 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Liu, Z. et al. Harnessing chemical energy for the activation and joining of prebiotic building blocks. Nat. Chem. 12, 1023–1028 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Foden, C. S. et al. Prebiotic synthesis of cysteine peptides that catalyze peptide ligation in neutral water. Science 370, 865–869 (2020).

    CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar
     

  • Schneider, C. et al. Noncanonical RNA nucleosides as molecular fossils of an early Earth—generation by prebiotic methylations and carbamoylations. Angew. Chem. Int. Ed. Engl. 57, 5943–5946 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Danger, G., Plasson, R. & Pascal, R. Pathways for the formation and evolution of peptides in prebiotic environments. Chem. Soc. Rev. 41, 5416–5429 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Bondalapati, S., Jbara, M. & Brik, A. Expanding the chemical toolbox for the synthesis of large and uniquely modified proteins. Nat. Chem. 8, 407–418 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Berg, P. The chemical synthesis of amino acyl adenylates. J. Biol. Chem. 233, 608–611 (1958).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Wu, L.-F., Su, M., Liu, Z., Bjork, S. J. & Sutherland, J. D. Interstrand aminoacyl transfer in a tRNA acceptor stem-overhang mimic. J. Am. Chem. Soc. 143, 11836–11842 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

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