Origin of Biological Homochirality by Crystallization of an RNA Precursor on a Magnetic Surface

Abstract

Homochirality is a signature of life on Earth yet its origins remain an unsolved puzzle. Achieving homochirality is essential for a high-yielding prebiotic network capable of producing functional polymers like ribonucleic acid (RNA) and peptides. However, a prebiotically plausible and robust mechanism to reach homochirality has not been shown to this date. The chiral-induced spin selectivity (CISS) effect has established a strong coupling between electron spin and molecular chirality and this coupling paves the way for breaking the chiral molecular symmetry by spin-selective processes. Magnetic surfaces can act as chiral agents due to the CISS effect and they can be templates for the enantioselective crystallization of chiral molecules. Here we studied the spinselective crystallization of racemic ribo-aminooxazoline (RAO), an RNA precursor, on magnetite (Fe3O4) surfaces, achieving an unprecedented enantiomeric excess of about 60%. Following the initial enrichment, we then obtained homochiral crystals of RAO after a subsequent crystallization. Our work combines two necessary features for reaching homochirality: chiral symmetry-breaking induced by the magnetic surface and self-amplification by conglomerate crystallization of RAO. Our results demonstrate a prebiotically plausible way of achieving systems level homochirality from completely racemic starting materials.

Chirality-Induced Magnetization of Magnetite by an RNA Precursor

“…Likewise, electrons with a well-deőned spin alignment to the molecular frame interact with chiral molecules based on their molecular handedness [15,16,17,18,19]. In our latest work, we reached homochirality utilizing this phenomenon and showed the importance of magnetic surfaces to induce enantioselective processes in a prebiotic network [20].…”

“…This natural net magnetization is not uniform albeit statistically significant and can allow for spin-selective asymmetric processes due to the CISS effect. In our previous work, we have shown that an essential RNA precursor, ribose-aminooxazoline (RAO), can selectively crystallize from a racemic mixture of pentose aminooxazolines on a magnetized magnetite (Fe3O4) surface[20]. Although, with a subsequent re-crystallization, we obtained nearly enantiopure crystals of RAO; in a natural environment, on a surface with non-uniform magnetization, this process will inevitably be less selective.…”

“…Moreover, we have shown that, conglomerate crystallization can accompany the chiral symmetry breaking by the magnetic surface as a simultaneous and well-matched ampliőcation mechanism. By combining these two necessary features to reach homochirality, we obtained enantiopure crystals of ribose-aminooxazoline (RAO) on magnetite surfaces, from a fully racemic solution of RAO [20]. RAO is a ribonucleotide precursor that can be synthesized by the reaction of glyceraldehyde and 2-aminooxazole with high-yields under prebiotically plausible conditions [22,23].…”

“…It is a poorly water-soluble compound that is stable against racemization and forming homochiral crystals in the non-centrosymmetric P2 1 2 1 2 1 space group [24,22,25]. Last but not least, the emergence of homochirality at the stage of RAO allows for the propagation of homochirality through RNA to peptides and therefore to the entire prebiotic network [26,27,20]. With these features, RAO is an important prebiotic compound which can play a central role in the origin of homochirality.…”

“…Our previous results on spin-selective crystallization of RAO on Fe 3 O 4 surfaces demonstrate that it is possible to obtain enantiopure RAO from a racemic mixture by a process controlled only by the environ-ment [20]. However, the interaction behind this process is not one-sided: just as magnetic surfaces induce enantioselective processes among chiral molecules, chiral molecules as well can induce spin polarization on magnetic surfaces.…”