Searching for lost nucleotides of the pre-RNA World with a self-refining model of early Earth

Abstract

The nucleotides of RNA appear to be products of evolution. Experimental studies are showing that plausible proto-nucleotides can be formed in simulated early Earth environments. In turn, these results help to clarify the prebiotic processes that give rise to nucleotides.

Fig. 1

The RNA nucleotides and a hypothetical process for prebiotic nucleotide and proto-RNA formation. a The extant RNA nucleotides. The name of each nucleobase is given above its respective nucleotide. The phosphate and ribose subunits of the adenine nucleotide are labeled to emphasize the modular molecular structure of nucleotides. b Schematic representation of prebiotic nucleotide synthesis and polymerization. The subunits of the prebiotic nucleotides are shown as nondescript molecular entities because their identities are unknown. Some functional groups of the extant nucleotides are shown on the prebiotic nucleotide subunits to emphasize that some chemical and structural features of the earliest nucleotides may have been retained over the course of evolution due to the constraints imposed by a requirement for forward compatibility, such as the ability to form Watson-Crick, or similar, base pairs. The reversibility of nucleotide formation and polymerization, indicated by reverse arrows, emphasizes our hypothesis that early nucleotides and proto-RNA polymers would have had linkages that were more thermodynamically favored and less kinetically trapped compared to the extant nucleotides and nucleic acids

Fig. 2

Illustration of an early Earth environment considered most favorable for nucleotide formation. From top to bottom: Precursors for the synthesis of the organic subunits of nucleotides are formed in the atmosphere of the early Earth with energy provided by photons and solar energetic particles (e.g., high energy protons from the young Sun). These precursors include formaldehyde, HCN, the products of HCN reacting with water (i.e., formamide and ammonium formate), urea, as well as others not listed. Precipitation brings these molecules along with water to the surface of the Earth. Urea is concentrated in low-lying regions on the surface of the Earth due to its high production, chemical stability, solubility in water, and low volatility. Solutions containing high concentrations of urea, other dissolved organics, and phosphate provide the subunits of prebiotic nucleotides. These subunits form dehydration condensation bonds to create nucleotides during times of low water activity and elevated temperatures