Evolutionary Biology pp 3-22 | Cite as
Spontaneous Generation Revisited at the Molecular Level
Abstract
A homogeneous chemical frame is described allowing one-pot syntheses from the one-carbon compound formamide NH2CHO to the whole set of nucleic bases needed as precursors of nucleic acids, as we know them. Formamide also catalyzes the formation of acyclonucleosides and the phosphorylation of nucleosides to nucleotides.
The conditions are described in which the survival of these prebiotically plausible nucleotides is favored. The scenario is simple: the polymeric forms are thermodynamically favored over the monomeric ones. The consequences of this very property are relevant: the formation and the accumulation of (pre)genetic information.
Keywords
Phosphodiester Bond Cyclic Form Spontaneous Generation Nucleic Basis Copper PhosphateNotes
Acknowledgments
This work is supported by the Italian Space Agency “MoMa project,” by ASI-INAF n. I/015/07/0 “Esplorazione del Sistema Solare,” Italy and by “The National Science Foundation,” USA (CBC Program).
References
- Bibillo A, Figlerowicz M, Kierzek R (1999) The non-enzymatic hydrolysis of oligoribonucleotides. VI. The role of biogenic polyamines. Nucleic Acids Res 27:3931–3937Google Scholar
- Biondi E, Branciamore S, Maurel MC, Gallori E (2007) Montmorillonite protection of an UV-irradiated hairpin ribozyme: evolution of the RNA world in a mineral environment. BMC Evol Biol 7 (Suppl 2):S2Google Scholar
- Ciciriello F, Costanzo G, Pino S, Crestini C, Saladino R, Di Mauro E (2008) Molecular complexity favors the evolution of ribopolymers. Biochemistry 47:2732–2742CrossRefPubMedGoogle Scholar
- Costanzo G, Saladino R, Crestini C, Ciciriello F, Di Mauro E (2007a) Nucleoside phosphorylation by phosphate minerals. J Biol Chem 282:16729–16735CrossRefPubMedGoogle Scholar
- Costanzo G, Saladino R, Crestini C, Ciciriello F, Di Mauro E (2007b) Formamide as main building block in the origin of life. BMC Evolutionary Biology 7 (Suppl 2):S1CrossRefPubMedGoogle Scholar
- Costanzo G, Pino S, Ciciriello F, Di Mauro E (2008) Nonenzymatic nucleoside phosphorylation and oligomerization in water. (submitted)Google Scholar
- Darwin F (1888) The life and letters of Charles Darwin, vol 3. John Murray, London, p 18 (letter to Joseph Hooker)Google Scholar
- Delaye L, Lazcano A (2005) Prebiological evolution and the physics of the origin of life. Phys Life Rev 2:47–64CrossRefGoogle Scholar
- Ferris JP, Ertem G (1993) Montmorillonite catalysis of RNA oligomer formation in aqueous solution. A model for the prebiotic formation of RNA. J Am Chem Soc 115:12270–12275Google Scholar
- Ferris JP, Hill AR Jr, Liu R, Orgel LE (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59–61CrossRefPubMedGoogle Scholar
- Ferris JP, Joshi PC, Wang KJ, Miyakawa S, Huang W (2004) Catalysis in prebiotic chemistry: application to the synthesis of RNA oligomers. Adv Space Res 33:100–105CrossRefGoogle Scholar
- Fuller WD, Sanchez RA, Orgel LE (1972) Studies in prebiotic synthesis: VII. Solid-state synthesis of purine nucleosides. J Mol Evol 1:249–257Google Scholar
- Gallori E, Biondi E, Branciamore S (2006) Looking for the primordial genetic honeycomb. Orig Life Evol Biosph 36:493–499CrossRefPubMedGoogle Scholar
- Huang W, Ferris JP (2003) Synthesis of 35–40 mers of RNA oligomers from unblocked monomers. A simple approach to the RNA world. Chem Commun (Camb) 12:1458–1459Google Scholar
- Holcomb DN, Tinoco I Jr (1965) Conformation of polyriboadenylic acid: pH and temperature dependence. Biopolymers 3: 121–133CrossRefGoogle Scholar
- Ito K, Sugawara T, Shiroishi M, Tokuda N, Kurokawa A, Misaka T, Makyio H, Yurugi-Kobayashi T, Shimamura T, Nomura N, Murata T, Abe K, Iwata S, Kobayashi T (2008) Advanced method for high-throughput expression of mutated eukaryotic membrane proteins in Saccharomyces cerevisiae. Biochem Biophys Res Commun 371:841–845CrossRefPubMedGoogle Scholar
- Joyce GF (1989) RNA evolution and the origins of life. Nature 338:217–224CrossRefPubMedGoogle Scholar
- Kanavarioti A, Monnard PA, Deamer DW. (2001) Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis. Astrobiology 1:271–281CrossRefPubMedGoogle Scholar
- Kaukinen U, Lyytikäinen S, Mikkola S, Lönnberg H. (2002) The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides strongly dependent on the base sequence. Nucleic Acids Res 30:468–467CrossRefPubMedGoogle Scholar
- Kawamura K, Ferris JP (1994) Kinetic and mechanistic analysis of dinucleotide and oligonucleotide formation from the 5′-phosphorimidazolide of adenosine on Na+-montmorillonite. J Am Chem Soc 116:7564–7572CrossRefPubMedGoogle Scholar
- Kierzek R (1992) Nonenzymatic hydrolysis of oligoribonucleotides. Nucleic Acids Res 20:5079–5084CrossRefPubMedGoogle Scholar
- Kozlov IA, Politis PK, Pitsch S, Herdewijn P, Orgel LE (1999) A highly enantio-selective hexitol nucleic acid template for nonenzymatic oligoguanylate synthesis. J Am Chem Soc 121:1108–1109CrossRefPubMedGoogle Scholar
- Li Y, Breaker RR (1999) Kinetics of RNA degradation by specific base catalysis of transesterification involving the 2′-hydroxyl group. J Am Chem Soc 121:5364–5372CrossRefGoogle Scholar
- Litovchick A, Szostak JW (2008) Selection of cyclic peptide aptamers to HCV IRES RNA using mRNA display. Proc Natl Acad Sci USA 105:15293–15298CrossRefPubMedGoogle Scholar
- Lohrmann R (1977) Formation of nucleoside 5′-phosphoramidates under potentially prebiological conditions. J Mol Evol 10:137–154CrossRefPubMedGoogle Scholar
- Mansy SS, Szostak JW (2008) Thermostability of model protocell membranes. Proc Natl Acad Sci USA 105:13351–13355CrossRefPubMedGoogle Scholar
- Mansy SS, Schrum JP, Krishnamurthy M, Tobé S, Treco DA, Szostak JW (2008) Template-directed synthesis of a genetic polymer in a model protocell. Nature 454:122–125CrossRefPubMedGoogle Scholar
- Millar TJ (2004) Organic molecules in the interstellar medium. In: Ehrenfreud P et al. (eds) Astrobiology: future perspectives. Kluwer, The Netherlands, pp 17–21Google Scholar
- Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117:528–529CrossRefPubMedGoogle Scholar
- Miller SL (1955) Production of some organic compounds under possible primitive Earth conditions. J Am Chem Soc 77:2351–2361CrossRefGoogle Scholar
- Monnard PA, Kanavarioti A, Deamer DW (2003) Eutectic phase polymerization of activated ribonucleotide mixtures yields quasi-equimolar incorporation of purine and pyrimidine nucleobases. J Am Chem Soc 125:13734–13740CrossRefPubMedGoogle Scholar
- Murtas G, Kuruma Y, Bianchini P, Diaspro A, Luisi PL (2007) Protein synthesis in liposomes with a minimal set of enzymes. Biochem Biophys Res Commun 363:12–17CrossRefPubMedGoogle Scholar
- Norberg J, Nilsson L (1995) Stacking free energy profiles for all 16 natural ribodinucleoside monophosphates in aqueous solution. J Am Chem Soc 117:10832–10840CrossRefGoogle Scholar
- Orgel LE (1998) The origin of life—a review of facts and speculations. Trends Biochem Sci 23:491–495CrossRefPubMedGoogle Scholar
- Orgel LE (2004) Prebiotic chemistry and the origin of the RNA world. Crit Rev Biochem Mol Biol 39:99–123CrossRefPubMedGoogle Scholar
- Oró J (1961a) Mechanism of synthesis of adenine from hydrogen cyanide under possible primitive earth conditions. Nature 191:1193–1194CrossRefPubMedGoogle Scholar
- Oró J (1961b) Comets and the formation of biochemical compounds on the primitive Earth. Nature 190:389–390CrossRefGoogle Scholar
- Oró J, Kimball A (1960) Synthesis of adenine from ammonium cyanide. Biochem Biophys Res Commun 2:407–412CrossRefGoogle Scholar
- Oró J, Kimball A (1961) Synthesis of purines under possible primitive earth conditions. I. Adenine from hydrogen cyanide. Arch Biochem Biophys 94:217–227Google Scholar
- Perreault DM, Anslyn EV (1997) Unifying the current data on the mechanism of cleavage-transesterification of RNA. Angew Chem Int Ed Engl 36:432–450CrossRefGoogle Scholar
- Pino S, Ciciriello F, Costanzo G, Di Mauro E (2008) Nonenzymatic RNA Ligation in Water. J Biol Chem 283:36494–36503CrossRefPubMedGoogle Scholar
- 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 38:57–74CrossRefPubMedGoogle Scholar
- Saladino R, Crestini C, Costanzo G, Negri R, Di Mauro E (2001) A possible prebiotic synthesis of purine, adenine, cytosine, and 4(3H)-pyrimidone from formamide: implications for the origin of life. Bioorg Med Chem 9:1249–1253CrossRefPubMedGoogle Scholar
- Saladino R, Ciambecchini U, Crestini C, Costanzo G, Negri R, Di Mauro E (2003) One-pot TiO2-catalyzed synthesis of nucleic bases and acyclonucleosides from formamide: implications for the origin of life. ChemBioChem 4:514–521CrossRefPubMedGoogle Scholar
- Saladino R Crestini C, Ciambecchini U, Ciciriello F, Costanzo G, Di Mauro E (2004) Synthesis and degradation of nucleobases and nucleic acids by formamide in the presence of montmorillonites. ChemBioChem 11:1558–1566CrossRefGoogle Scholar
- Saladino R, Crestini C, Busiello V, Ciciriello F, Costanzo G, Di Mauro E (2005) Origin of informational polymers. Differential stability of 3′- and 5′-phosphoester bonds in deoxy monomers and oligomers. J Biol Chem 280:35658–35669Google Scholar
- Saladino R, Crestini C, Neri V, Brucato J, Colangeli L, Ciciriello F, Di Mauro E, Costanzo G (2005) Synthesis and degradation of nucleic acids components by formamide and cosmic dust analogs. ChemBioChem 6:1368–1374CrossRefPubMedGoogle Scholar
- Saladino R, Crestini C, Ciciriello F, Di Mauro E, Costanzo G (2006a) Origin of informational polymers: differential stability of phosphoester bonds in ribomonomers and ribooligomers. J Biol Chem 281:5790–5796CrossRefPubMedGoogle Scholar
- Saladino R, Crestini C, Neri V, Ciciriello F, Costanzo G, Di Mauro E (2006b) Origin of informational polymers: the concurrent roles of formamide and phosphates. ChemBioChem 7:1707–1714CrossRefPubMedGoogle Scholar
- Saladino R, Crestini C, Ciciriello F, Costanzo G, Di Mauro E (2007) Formamide chemistry and the origin of informational polymers. Chem Biodivers, Helv Chim Acta 4:694–720Google Scholar
- Saladino R, Neri V, Crestini C, Costanzo G, Graciotti M, Di Mauro E (2008) Synthesis and degradation of nucleic acid components by formamide and iron sulphur minerals. J Am Chem Soc (Web Release Date: 22 October 2008); doi:10.1021/ja804782eGoogle Scholar
- Schwartz A (1997) Prebiotic phosphorus chemistry reconsidered. Origins Life Evol Biosph 27:505–512CrossRefGoogle Scholar
- Soukup GA, Breaker RR (1999a) Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5:1308–1325CrossRefPubMedGoogle Scholar
- Soukup GA, Breaker RR (1999b) Nucleic acid molecular switches. Trends Biotechnol 17:469–476CrossRefPubMedGoogle Scholar
- Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409:387–390CrossRefPubMedGoogle Scholar
- Tohidi M, Orgel LE (1989) Some acyclic analogs of nucleotides and their template-directed reactions. J Mol Evol 28:367–373CrossRefPubMedGoogle Scholar
- Toyota T, Takakura K, Kageyama Y, Kurihara K, Maru N, Ohnuma K, Kaneko K, Sugawara T (2008) Population study of sizes and components of self-reproducing giant multilamellar vesicles. Langmuir 24:3037–3044CrossRefPubMedGoogle Scholar
- van Holde KE (1980) The origin of life: a thermodynamic critique in “The origins of life and evolution.” In: Halvorson HO, van Holde KE (eds) The origins of life and evolution. Alan R. Liss, New York, pp 31–46Google Scholar
- Wächtershäuser G (1988) Before enzymes and templates, theory of surface metabolism. Microbiol Rev 52:452–484PubMedGoogle Scholar
- Walde P (2006) Surfactant assemblies and their various possible roles for the origin(s) of life. Orig Life Evol Biosph 36:109–150CrossRefPubMedGoogle Scholar
- Zubay G, Mui T (2001) Prebiotic synthesis of nucleotides. Origins Life Evol Biosph 31:87–102CrossRefGoogle Scholar