Molecular Complexity Favors the Evolution of Ribopolymers

Ciciriello, Fabiana; Costanzo, Giovanna; Pino, Samanta; Crestini, Claudia; Saladino, Raffaele; Mauro, Ernesto Di

doi:10.1021/bi7021014

Cited by 18 publications

(17 citation statements)

References 48 publications

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“…The half-life of RNA oligonucleotides in water has been a matter of detailed analyses (11,17). As expected, and based on a large body of previous studies, the observed half-life of RNA molecules depends on sequence composition, temperature, pH, and concentration.…”

Section: Increased Stability Of Rna Oligonucleotides In Water Is Causmentioning

confidence: 82%

Generation of Long RNA Chains in Water

Costanzo

Pino

Ciciriello

et al. 2009

Journal of Biological Chemistry

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120

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The synthesis of RNA chains from 3,5-cAMP and 3,5-cGMP was observed. The RNA chains formed in water, at moderate temperatures (40 -90°C), in the absence of enzymes or inorganic catalysts. As determined by RNase analyses, the bonds formed were canonical 3,5-phosphodiester bonds. The polymerizations are based on two reactions not previously described: 1) oligomerization of 3, 5-cGMP to ϳ25-nucleotide-long RNA molecules, and of 3,5-cAMP to 4-to 8-nucleotide-long molecules. Oligonucleotide A molecules were further extended by reciprocal terminal ligation to yield RNA molecules up to >120 nucleotides long and 2) chain extension by terminal ligation of newly polymerized products of 3,5-cGMP on preformed oligonucleotides. The enzyme-and template-independent synthesis of long oligomers in water from prebiotically affordable precursors approaches the concept of spontaneous generation of (pre)genetic information.The origin of informational polymers is not understood. The RNA polymerization process has been studied for five decades, the results showing that from preactivated precursors polymers of several tens can be obtained, as reviewed previously (1). These pioneering studies provide the proof-of-principle that RNA precursors can self-assemble yielding linear polymers. However, the prebiotic validity of a process based on complex preactivation procedures is limited (1, 2), and the problem of defining a prebiotically plausible chemical and thermodynamic scenario for the synthesis and accumulation of informational polymers remains open. The core of the problem is the standard state Gibbs free energy change (3, 4) stating that condensation reactions are very inefficient in water. Given that extant polymerizations occur in water, this is a major difficulty, only partially solved by the fact that these processes at present occur inside the active site of enzymes where water activity may be drastically reduced. The other part of the extant solution, fruit of evolution, is the use of biologically highly preactivated triphosphate nucleotides (3). In primordia, RNA molecules had no enzymes to catalyze their chain-wise growth, and highly activated precursors can be considered as prebiotic only with difficulty.We reasoned that for a pre-enzymatic polymerization to occur the solution must have relied on a simple and robust process. Ideally, such a process should have been based on compounds that were reactive yet relatively stable, chemically not too elaborate to allow their efficient production, and not too dissimilar from the products of their polymerization to minimize the chemical cost of the process.It was observed that phosphorylation of nucleosides occurs in formamide simply in the presence of a source of organic or inorganic phosphate at temperatures at which both the reactants and the products are stable (5). Phosphorylation occurs in every possible position of the nucleoside sugar moiety resulting, both for purine and pyrimidine nucleosides, in the production of 2Ј-, 3Ј-, 5Ј-, 2Ј,3Ј-cyclic, and 3Ј,5Ј-cyclic XMPs 3 (5). Th...

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Section: Increased Stability Of Rna Oligonucleotides In Water Is Causmentioning

confidence: 82%

Generation of Long RNA Chains in Water

Costanzo

Pino

Ciciriello

et al. 2009

Journal of Biological Chemistry

Self Cite

120

138

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“…This particular physical-chemical setting was selected because RNA degradation in these conditions takes reasonable experimental time span, as previously detailed [15,16], and because of its per se interest in a prebiotic perspective [17]. A preliminary set of analyses consisted in (i) the determination of the stability of borate minerals at 80 °C in water or in formamide and in (ii) the measurement of the variation of pH induced by minerals in the aqueous environment.…”

Section: The Rna Stability Assaymentioning

confidence: 99%

“…Nucleic acid base-stacking is at present an understood phenomenon [24][25][26][27][28]. The possibility that the initial stability of the PolyA oligonucleotide towards hydrolysis is a base stacking-related effect was discussed in [15]. Table 3, showed that the large majority of the minerals analyzed caused faster degradation of the polymeric form, both in water and in formamide.…”

Section: Rna Stability In Boron Mineralsmentioning

confidence: 99%

“…The degradation of RNA oligonucleotides in water is a well studied process [15,[30][31][32]. The degradation reaction in formamide was also described [16,17 and refs.…”

Section: The Rna Stability Assaymentioning

confidence: 99%

“…In RNA the key bond is the 3' phosphoester bond. It was noted that under defined physical-chemical conditions (namely: 60-90 °C in water) this bond is more stable by one order of magnitude in the polymer than in the monomer [15,29,42]. This observation establishes a principle but is not sufficient to account for the origin of long polymers.…”

Section: The Survival Of Polymers In Unprotected Abiotic Environmentmentioning

confidence: 99%

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Borate Minerals and RNA Stability

et al. 2010

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Abstract:The abiotic origin of genetic polymers faces two major problems: a prebiotically plausible polymerization mechanism and the maintenance of their polymerized state outside a cellular environment. The stabilizing action of borate on ribose having been reported, we have explored the possibility that borate minerals stabilize RNA. We observe that borate itself does not stabilize RNA. The analysis of a large panel of minerals tested in various physical-chemical conditions shows that in general no protection on RNA backbone is exerted, with the interesting exception of ludwigite (Mg 2 Fe 3 +BO 5 ). Stability is a fundamental property of nucleic polymers and borate is an abundant component of the planet, hence the prebiotic interest of this analysis.

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Emergence of the First Catalytic Oligonucleotides in a Formamide‐Based Origin Scenario

Šponer

Nováková

et al. 2016

Chemistry A European J

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50 years after the historical Miller-Urey experiment, the formamide-based scenario is perhaps the most powerful concurrent hypothesis for the origin of life on our planet besides the traditional HCN-based concept. The information accumulated during the last 15 years in this topic is astonishingly growing and nowadays the formamide-based model represents one of the most complete and coherent pathways leading from simple prebiotic precursors up to the first catalytically active RNA molecules. In this work, we overview the major events of this long pathway that have emerged from recent experimental and theoretical studies, mainly concentrating on the mechanistic, methodological, and structural aspects of this research.

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Molecular Complexity Favors the Evolution of Ribopolymers

Cited by 18 publications

References 48 publications

Generation of Long RNA Chains in Water

Generation of Long RNA Chains in Water

Borate Minerals and RNA Stability

Emergence of the First Catalytic Oligonucleotides in a Formamide‐Based Origin Scenario

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