Chirality in the RNA world and beyond

Homochirality is an essential feature of biology, but how it developed in early life remains unclear. Our aim in this paper is to add to the discussion by taking a somewhat arbitrary but definite sequence of events and examining carefully the chirality at each stage. Our scenario for the development of life starts with the prebiotic, continues through a pre-RNA stage to the RNA world. This leads to the development of proteins and then to the incorporation of DNA in RNA-DNA-protein biochemistry. We argue that homochirality probably did not develop prebiotically. We see the likely chiral bifurcation point to be during the development of RNA from an achiral pre-RNA. Surprisingly, we find the driving force for this to be enantiomeric cross-inhibition in which the addition of a 'wrong-handed' enantiomer to a growing polymer brings the polymerization to a halt. This, it is often argued, is a serious impediment to the development of chiral purity. We suggest that the sign of handedness at this stage was probably determined by chance. We then point out that homochiral RNA was unlikely by itself to lead to homochiral proteins. We identify the additional nonlinear feature required for bifurcation to be the rapid increase in enzymic power available when the amino acids in proteins approach single handedness and structural features such as alpha-helices and beta-sheets become viable. If this is correct, then the handedness of the protein sector is indeed linked to that of RNA. However, the relative sign of the two handednesses will have depended on the precise stereo-sensitive interaction between the RNA and protein systems. We suggest that the most plausible scenario is via the recently discovered RNA binding sites for amino acids, which are both stereo-selective and have contact with the developing genetic code. The detailed steps that determine the handedness are not yet clear and may be specific to the precise development path. It follows that if biochemistry similar to that on Earth developed extraterrestrially, we would surely have homochirality but at this stage we cannot be sure about the handedness of either the nucleic acid or the protein components. Received 7 March 2005, accepted 15 May 2005