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New evolutionary insights into the non‐enzymatic origin of RNA oligomers

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We outline novel findings on the non‐enzymatic polymerization of nucleotides under plausible prebiotic conditions and on the spontaneous onset of informational complexity in the founding molecule, RNA. We argue that the unique ability of 3′, 5′ cyclic guanosine monophosphate to form stacked architectures and polymerize in a self‐sustained manner suggests that this molecule may serve as the ‘seed of life’ from which all self‐replicating oligonucleotides can be derived via a logically complete sequence of simple events. WIREs RNA 2017, 8:e1400. doi: 10.1002/wrna.1400 This article is categorized under: RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution
Molecular geometry of 3′, 5′ cGMP as determined by X‐ray crystallography.
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Transiently stabilized tetraloop‐like overhangs may mediate transphosphorylation reactions leading to ligation, cleavage, and terminal recombination reactions, a primitive form of RNA‐catalysis.
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The 3′, 5′ cGMPs as ‘seeds’ of ancient oligonucleotides. Living polymerization of 3′, 5′ cGMPs is made possible by their intrinsic ability to form stacked architectures. OligoGs, produced by the oligomerization of 3′, 5′ cGMPs could serve as templates for their own replication. Further, H‐bonding between oligoG templates and 3′, 5′ cCMPs could induce the formation of oligoC sequences. The combination of H‐bonding and stacking interactions could lead to ligation and terminal recombination reactions between oligoG and oligoC sequences producing mixed C‐ and G‐containing oligonucleotides. cGMP = 3′, 5′ cGMP, cCMP = 3′, 5′ cCMP.
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The symmetry of the stacked architecture formed from 3′, 5′ cGMPs enables serial transphosphorylations between both the right and left hand side nucleotides.
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Molecular and crystal geometry of the thio‐substituted variant of 2′, 3′ cyclic uridine monophosphate as determined by X‐ray diffraction.
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Nucleotide‐packing in the crystals of 3′, 5′ cyclic nucleotides. While crystals of 3′, 5′ cGMP are primarily stabilized by stacking interactions, the self‐assembly of 3′, 5′ cAMPs is also supported by H‐bonding. Conversely, the dominant intermolecular force stabilizing the crystals of 3′, 5′ cUMP (uridine 3′, 5′ cyclic monophosphate) is H‐bonding.
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Mechanism of the anionic ring‐opening polymerization of 3′, 5′ cGMPs. The oligomerization is initiated by the high‐pH‐induced hydrolysis of a cyclic nucleotide that leads to an O3′‐deprotonated nucleotide. The anionic 3′‐oxygen of this nucleotide is optimally positioned to attack the next phosphate in the stacked architecture. This step then recurs, leading to selectively 3′, 5′‐linked oligomers.
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