Survival of the fittest before the beginning of life: selection of the first oligonucleotide-like polymers by UV light

Abstract

Background: A key event in the origin of life on this planet has been formation of self-replicating RNA-type molecules, which were complex enough to undergo a Darwinian-type evolution (origin of the "RNA world"). However, so far there has been no explanation of how the first RNA-like biopolymers could originate and survive on the primordial Earth.

Results: As condensation of sugar phosphates and nitrogenous bases is thermodynamically unfavorable, these compounds, if ever formed, should have undergone rapid hydrolysis. Thus, formation of oligonucleotide-like structures could have happened only if and when these structures had some selective advantage over simpler compounds. It is well known that nitrogenous bases are powerful quenchers of UV quanta and effectively protect the pentose-phosphate backbones of RNA and DNA from UV cleavage. To check if such a protection could play a role in abiogenic evolution on the primordial Earth (in the absence of the UV-protecting ozone layer), we simulated, by using Monte Carlo approach, the formation of the first oligonucleotides under continuous UV illumination. The simulations confirmed that UV irradiation could have worked as a selective factor leading to a relative enrichment of the system in longer sugar-phosphate polymers carrying nitrogenous bases as UV-protectors. Partial funneling of the UV energy into the condensation reactions could provide a further boost for the oligomerization.

Conclusion: These results suggest that accumulation of the first polynucleotides could be explained by their abiogenic selection as the most UV-resistant biopolymers.

Figure 1

Schematic representation of the modeled reactions

Figure 2

Monte Carlo simulation of a sugar-phosphate polymerization reaction in the presence of nitrogenous bases and under UV-illumination Sugar-phosphate polymerization reaction in the presence of nitrogenous bases and under UV-illumination was simulated using the following parameter set: The concentration of monomers in the reaction volume was kept on a constant level of 10^-3 M (comparable with their concentration in the cell). The second-order rate constant of polymerization k_poly was 3 M^-1 s^-1 and the first-order rate constant of re-dissociation k_mono was 10^-4 s^-1 that corresponded to the equilibrium constant = 30. The rate constants of nucleotide binding (k_bind) and dissociation (k_diss) were 3 × 10^-8 s^-1 and 10^-6 s^-1, respectively ( = 3 × 10^-2). Under the UV illumination, monomers decomposed with the rate constant of 3·10^-3 s^-1 irrespectively of their position in the chain. For simplicity, the UV protection factor U of 30 was used both for monomers and oligomers. The partial funneling of UV energy was assumed to increase the k_bind value from 3 × 10^-8s^-1 up to 1.2 × 10^-7 s^-1. a, Polymer length distribution at equilibrium. b, Fraction of monomers protected by nitrogenous bases as a function of time.