Water cycles in a Hadean CO2 atmosphere drive the evolution of long DNA

Abstract

Dew is a common form of water that deposits from saturated air on colder surfaces. Although presumably common on primordial Earth, its potential involvement in the origin of life in early replication has not been investigated in detail. Here we report that it can drive the first stages of Darwinian evolution for DNA and RNA, first by periodically denaturing their structures at low temperatures and second by promoting the replication of long strands over short, faster replicating ones. Our experiments mimicked a partially water-filled primordial rock pore in the probable CO2 atmosphere of Hadean Earth. Under heat flow, water continuously evaporated and recondensed as acidic dew droplets that created the humidity, salt and pH cycles that match many prebiotic replication chemistries. In low-salt and low-pH regimes, the strands melted at 30 K below the bulk melting temperature, whereas longer sequences preferentially accumulated at the droplet interface. Under an enzymatic replication to mimic a sped-up RNA world, long sequences of more than 1,000 nucleotides emerged. The replication was biased by the melting conditions of the dew and the initial short ATGC strands evolved into long AT-rich sequences with repetitive and structured nucleotide composition.

RNA polymerisation without catalyst from 2’,3’-cyclic nucleotides by drying at air-water interfaces

“…Moreover, we have shown that efficient strand separation can be achieved by low sodium concentrations, triggered by microscale water cycles within heated rock pores. [35,36] Our very preliminary digestion studies suggest a considerable backbone heterogeneity (2´-5´ and 3´-5´) within the polymers. However, a full quantitative treatment is beyond the scope of this study.…”

“…A length-selective enzymatic DNA replication was reported recently within this setting, indicating the possible continuity of prebiotic chemistry in such a setting. [36] We observed all the dimer sequence combinations and most of the trimers (Figure 3c). However, the tetramers and pentamers show sequences rich in G. The length selectivity of the HPLC allowed the detection of longer sequences, but the isotopic fit to the raw mass spectra provided by our LabView-based analysis showed that longer species with concentrations lower than 0.2 µM were lost in the background noise of the mass spectra.…”

“…We also showed polymerisation in the wet-dry cycling environment at a heated air-water interface, adding RNA polymerisation to the pool of prebiotic processes possible within such a setting. [34][35][36] Under the tested conditions, the reaction yielded polymers up to 15-mers. The formed polyG incorporated cCMP, cAMP and cUMP monomers, albeit in lower concentration, which did not homopolymerise significantly.…”

“…We have previously reported prebiotically important processes such as accumulation, phosphorylation, encapsulation, gelation, strand separation, enzymatic DNA replication and crystallisation within such settings. [34][35][36] For the polymerisation within this setting, we started with 20 mM total monomers (5 mM each of cG, cC, cA and cU). After the chamber was loaded with the monomer solution, a thermal gradient was applied which drove a continuous wet-dry cycle just above the air-water interface inside the chamber (Figure 3a).…”

“…The dew droplets grew at the cooler side of the chamber and upon contact with the warm side, the dew rehydrated the dried material and transports it back into the bulk mostly due to bubble fusion driven by surface tension. [36] This phenomenon was allowed to continue for 18 hours, after which the setup was dismounted and the remaining bulk liquid and the dried flakes (after dissolution) were sampled for analysis.…”