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Journal of Molecular Evolution

, Volume 82, Issue 1, pp 5–10 | Cite as

Four Ways to Oligonucleotides Without Phosphoimidazolides

  • Judit E. ŠponerEmail author
  • Jiří Šponer
  • Ernesto Di Mauro
Original Article

Abstract

Emergence of the very first RNA or RNA-like oligomers from simple nucleotide precursors is one of the most intriguing questions of the origin of life research. In the current paper, we analyse the mechanism of four non-enzymatic template-free scenarios suggested for the oligomerization of chemically non-modified cyclic and acyclic nucleotides in the literature. We show that amines may have a twofold role in these syntheses: due to their high affinity to bind protons they may activate the phosphorus of the phosphate group via proton transfer reactions, or indirectly they may serve as charge compensating species and influence the self-assembling of nucleotides to supramolecular architectures compatible with the oligomerization reactions. Effect of cations and pH on the reactions is also discussed.

Keywords

RNA Polymerization Origin of life Oligonucleotides 

Notes

Acknowledgments

Financial support from the grant GAČR 14-12010S and from the project “CEITEC − Central European Institute of Technology” (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund is gratefully acknowledged. This work was supported by Italian Space Agency Project “Esobiologia e Ambienti Estremi: Dalla Chimica delle Molecola alla Biologia degli Estremofili” Number 2014-026-R.0 (Codice Unico Progetto F 92I14000030005).

Supplementary material

239_2015_9709_MOESM1_ESM.pdf (516 kb)
Supplementary material 1 (pdf 516 kb)

References

  1. Allen F (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr Sect B Struct Sci Cryst Eng Mat 58:380–388CrossRefGoogle Scholar
  2. Barone V, Cossi M (1998) Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model. J Phys Chem A 102:1995–2001CrossRefGoogle Scholar
  3. Beaucage SL, Caruthers MH (1981) Deoxynucleoside phosphoramidites—a new class of key intermediates for deoxypolynucleotide synthesis. Tetrahedron Lett 22:1859–1862CrossRefGoogle Scholar
  4. Chwang AK, Sundaralingam M (1974) The crystal and molecular structure of guanosine 3′,5′-cyclic monophosphate (cyclic GMP) sodium tetrahydrate. Acta Crystallogr B 30:1233–1240CrossRefGoogle Scholar
  5. Cossi M, Rega N, Scalmani G, Barone V (2003) Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J Comput Chem 24:669–681PubMedCrossRefGoogle Scholar
  6. Costanzo G, Pino S, Ciciriello F, Di Mauro E (2009) Generation of long RNA chains in water. J Biol Chem 284:33206–33216PubMedPubMedCentralCrossRefGoogle Scholar
  7. Costanzo G, Saladino R, Botta G, Giorgi A, Scipioni A, Pino S, Di Mauro E (2012) Generation of RNA molecules by a base-catalysed click-like reaction. ChemBioChem 13:999–1008PubMedCrossRefGoogle Scholar
  8. Da Silva L, Maurel MC, Deamer D (2015) Salt-promoted synthesis of RNA-like molecules in simulated hydrothermal conditions. J Mol Evol 80:86–97PubMedCrossRefGoogle Scholar
  9. DeGuzman V, Vercoutere W, Shenasa H, Deamer D (2014) Generation of oligonucleotides under hydrothermal conditions by non-enzymatic polymerization. J Mol Evol 78:251–262PubMedCrossRefGoogle Scholar
  10. Hill A Jr, Orgel L, Wu T (1993) The limits of template-directed synthesis with nucleoside-5′-phosphoro(2-methyl)imidazolides. Orig Life Evol Biosph 23:285–290PubMedCrossRefGoogle Scholar
  11. Jauker M, Griesser H, Richert C (2015) Spontaneous formation of RNA strands, peptidyl RNA, and cofactors. Angew Chem Int Ed. doi: 10.1002/anie.201506593 Google Scholar
  12. Kraut J, Jensen LH (1963) Refinement of the crystal structure of adenosine-5′-phosphate. Acta Crystallogr 16:79–88CrossRefGoogle Scholar
  13. Liu Y, Gregersen BA, Lopez X, York DM (2005) Density functional study of the in-line mechanism of methanolysis of cyclic phosphate and thiophosphate esters in solution: insight into thio effects in RNA transesterification. J Phys Chem B 109:19987–20003PubMedCrossRefGoogle Scholar
  14. Morasch M, Mast CB, Langer JK, Schilcher P, Braun D (2014) Dry polymerization of 3′,5′-cyclic GMP to long strands of RNA. ChemBioChem 15:879–883PubMedCrossRefGoogle Scholar
  15. Parker ET et al (2011) Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge experiment. Proc Natl Acad Sci USA 108:5526–5531PubMedPubMedCentralCrossRefGoogle Scholar
  16. Pearlman DA, Kim S-H (1985) Determinations of atomic partial charges for nucleic acid constituents from x-ray diffraction data. I. 2′-Deoxycytidine-5′-monophosphate. Biopolymers 24:327–357PubMedCrossRefGoogle Scholar
  17. Perras FA, Korobkov I, Bryce DL (2012) 23Na double-rotation NMR of sodium nucleotides leads to the discovery of a new dCMP hendecahydrate. Phys Chem Chem Phys 14:4677–4681PubMedCrossRefGoogle Scholar
  18. Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–242PubMedCrossRefGoogle Scholar
  19. Powner MW, Sutherland JD, Szostak JW (2011) The origins of nucleotides. Synlett 22:1956–1964CrossRefGoogle Scholar
  20. Rajamani S, Vlassov A, Benner S, Coombs A, Olasagasti F, Deamer D (2008) Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig Life Evol Biosph 38:57–74PubMedCrossRefGoogle Scholar
  21. Saladino R, Botta G, Pino S, Costanzo G, Di Mauro E (2012a) From the one-carbon amide formamide to RNA all the steps are prebiotically possible. Biochimie 94:1451–1456PubMedCrossRefGoogle Scholar
  22. Saladino R, Botta G, Pino S, Costanzo G, Di Mauro E (2012b) Genetics first or metabolism first? The formamide clue. Chem Soc Rev 41:5526–5565PubMedCrossRefGoogle Scholar
  23. Schrum JP, Ricardo A, Krishnamurthy M, Blain JC, Szostak JW (2009) Efficient and rapid template-directed nucleic acid copying using 2′-amino-2′,3′-dideoxyribonucleoside−5′-phosphorimidazolide monomers. J Am Chem Soc 131:14560–14570PubMedPubMedCentralCrossRefGoogle Scholar
  24. Silverton JV, Limn W, Miles HT (1982) 2-Amino-8-methyladenosine 5′-monophosphate dihydrate. A nucleotide with syn C4′-exo conformation and “triple-stranded” packing. J Am Chem Soc 104:1081–1087CrossRefGoogle Scholar
  25. Sponer JE, Sponer J, Giorgi A, Di Mauro E, Pino S, Costanzo G (2015) Untemplated nonenzymatic polymerization of 3′,5′cGMP: a plausible route to 3′,5′-linked oligonucleotides in primordia. J Phys Chem B 119:2979–2989PubMedCrossRefGoogle Scholar
  26. Sundaralingam M (1966) Stereochemistry of nucleic acid constituents. III. Crystal and molecular structure of adenosine 3′-phosphate dihydrate (adenylic acid b). Acta Crystallogr 21:495–506PubMedCrossRefGoogle Scholar
  27. Sundaralingam M, Prusiner P (1978) Zwitterionic character of nucleotides: possible significance in the evolution of nucleic acids. Nucleic Acids Res 5:4375–4383PubMedPubMedCentralCrossRefGoogle Scholar
  28. Szostak J (2012) The eightfold path to non-enzymatic RNA replication. J Syst Chem 3:2CrossRefGoogle Scholar
  29. Usher DA, Yee D (1979) Geometry of the dry-state oligomerization of 2′,3′-cyclic phosphates. J Mol Evol 13:287–293PubMedCrossRefGoogle Scholar
  30. Verlander MS, Lohrmann R, Orgel LE (1973) Catalysts for self-polymerization of adenosine cyclic 2′,3′-phosphate. J Mol Evol 2:303–316PubMedCrossRefGoogle Scholar
  31. von Kiedrowski G, Wlotzka B, Helbing J, Matzen M, Jordan S (1991) Parabolic growth of a self-replicating hexadeoxynucleotide bearing a 3′,5′-phosphoamidate linkage. Angew Chem Int Ed 30:423–426CrossRefGoogle Scholar
  32. Zielinski WS, Orgel LE (1987) Autocatalytic synthesis of a tetranucleotide analog. Nature 327:346–347PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Judit E. Šponer
    • 1
    • 2
    Email author
  • Jiří Šponer
    • 1
    • 2
  • Ernesto Di Mauro
    • 3
  1. 1.Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.CEITEC - Central European Institute of TechnologyMasaryk UniversityBrnoCzech Republic
  3. 3.Dipartimento di Biologia e Biotecnologie “Charles Darwin”“Sapienza” Università di RomaRomeItaly

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