Abiotic RNA Formation in Natural Nanoconfinements of Water: Overcoming the Water Paradox via a Nanofluidic Bridge Between Geochemistry and Biochemistry

<p class="western">The "water paradox" is an obstinate problem in the research on the chemical evolution towards the emergence of life. It states that although aqueous environments are essential for life, they hamper key condensation reactions such as nucleotide polymerisation. To overcome this paradox several hypotheses have been proposed, including scenarios based on alternative solvents like formamide, condensing agents like cyanamide, high temperatures of over 150 °C or wet/dry cycles in surface ponds. However, when appraising the prebiotic plausibility of such scenarios some general weaknesses appear. Besides the fact that all known life manages the water paradox without needing such proposed conditions, the principle that evolution builds on existing pathways indicates that the same physicochemical effects were probably involved in the abiotic origin of biopolymers as now being tapped by life via complex enzymes.</p> <p class="western">Here we show that abiotic temporal nanoconfinements of water can act as natural reactions vessels for prebiotic RNA formation. We present evidence for spontaneous, abiotic polymerisation of nucleotides in water. According to our results the reaction is enabled by the rise of anomalous properties of water when being temporarily confined between nanoscale separated particles of geological ubiquity within aqueous suspensions. These findings can solve the water paradox in such a way that nanofluidic effects in aqueous particle suspensions open up an abiotic route to biopolymerisation and polymer stabilisation under chemical and thermodynamic conditions which also exist within the intracellular environment of living cells. The fact that polymerase enzymes also form temporal nanoconfined water clusters inside their active site implies that the same physico-chemical effects are tapped for nucleotide condensation in water both by biochemical pathways and the reported abiotic route. This indicates that our model is consistent with evolutionary conservatism stretching back to the era of prebiotic chemical evolution. The consistency is further supported by the fact that water is not trapped by nanoconfinements within the polymerase core but can exchange with the surrounding intracellular fluid – a situation which is also prevalent in nanofluidic environments within aqueous particle suspensions. Our experimental finding that under the reported conditions an amino acid catalyses the abiotic polymerisation of nucleotides may give a hint to a nanofluidic origin of cooperation between amino acids and nucleotides evolving to the interdependent synthesis of proteins and nucleic acids in living cells.</p> <p class="western">The effect of abiotic RNA polymerisation in temporal nanoconfined water does not depend on highly specific mineral species and geological environments as watery suspensions of micro- and nanoparticles are virtually ubiquitous – they exist, for example, in the form of sediments with pore water, hydrothermal vent fluids containing precipitated inorganic and polyaromatic particles or dispersed aggregates inside water-filled cracks in the crust of the earth and possibly of icy moons in the outer solar system.</p> <p class="western"><strong>References</strong></p> <p class="western">Greiner de Herrera, A., Markert, T. & Trixler, F. Temporal nanofluidic confinements induce prebiotic condensation in water. Preprint, DOI: 10.21203/rs.3.rs-163645/v3</p>

Temporal nanofluidic confinements induce prebiotic condensation in water

A long-standing, crucial problem in the research on the chemical evolution towards the origin of life is the so-called ‘water paradox’. It states that although water is essential to life, key chemical reactions such as the synthesis of RNA are inhibited by it. Current hypotheses addressing this paradox have low prebiotic plausibility when taking the conservative nature of evolution into account. Here, we report spontaneous abiotic RNA formation in aqueous environments. The synthesis is driven by nanofluidic phenomena that alter critical properties of water. Our findings provide a solution to the paradox in a multifaceted way: abiotic, temporal nanofluidic confinements allow prebiotic condensation reaction pathways in water under stable, moderate conditions, emerge in aqueous particle suspensions as a geologically ubiquitous and thus prebiotic highly plausible environment and are consistent with the principle that evolution builds on existing pathways, as living cells also work with temporal nanoconfined water.

Temporal nanofluidic confinements induce prebiotic condensation in water

A long-standing, crucial problem in the research on the chemical evolution towards the origin of life is the so-called ‘water paradox’. It states that although water is essential to life, key chemical reactions such as the synthesis of RNA are inhibited by it. Current hypotheses addressing this paradox have low prebiotic plausibility when taking the conservative nature of evolution into account. Here, we report spontaneous abiotic RNA formation in aqueous environments. The synthesis is driven by nanofluidic phenomena that alter critical properties of water. Our findings provide a solution to the paradox in a multifaceted way: abiotic, temporal nanofluidic confinements allow prebiotic condensation reaction pathways in water under stable, moderate conditions, emerge in aqueous particle suspensions as a geologically ubiquitous and thus prebiotic highly plausible environment and are consistent with the principle that evolution builds on existing pathways, as living cells also work with temporal nanoconfined water.

Abiotic nanofluidic environments induce prebiotic condensation in water

A long-standing, central problem in the research on the chemical evolution towards the origin of life is the so-called “water paradox”: Despite life depends on liquid water, key biochemical reactions such as nucleotide condensation are inhibited by it. Current hypotheses addressing this paradox have low prebiotic plausibility when taking the conservative nature of evolution into account. We report spontaneous, abiotic RNA synthesis in water driven by nanofluidic effects in temporal nanoconfinements of aqueous particle suspensions. Our findings provide a solution of the water paradox in a multifaceted way: abiotic, temporal nanofluidic environments allow prebiotic condensation reaction pathways in water under stable, moderate conditions, emerge in suspensions as a geologically ubiquitous and thus prebiotic highly plausible environment and are consistent with evolutionary conservatism as living cells also work with temporal nanoconfined water.

Prebiotic condensation through wet–dry cycling regulated by deliquescence

Wet–dry cycling is widely regarded as a means of driving condensation reactions under prebiotic conditions to generate mixtures of prospective biopolymers. A criticism of this model is its reliance on unpredictable rehydration events, like rainstorms. Here, we report the ability of deliquescent minerals to mediate the oligomerization of glycine during iterative wet–dry cycles. The reaction mixtures evaporate to dryness at high temperatures and spontaneously reacquire water vapor to form aqueous solutions at low temperatures. Deliquescent mixtures can foster yields of oligomerization over ten-fold higher than non-deliquescent controls. The deliquescent mixtures tightly regulate their moisture content, which is crucial, as too little water precludes dissolution of the reactants while too much water favors hydrolysis over condensation. The model also suggests a potential reason why life evolved to favor the enrichment of potassium: so living systems could acquire and retain sufficient water to serve as a solvent for biochemical reactions.