On the origin of the mitochondrial genetic code: Towards a unified mathematical framework for the management of genetic information

Diego Luis Gonzalez,Rodolfo Rosa,Simone Giannerini

doi:10.1038/npre.2012.7136.1

Abstract

AbstractThe origin of the genetic code represents one of the most challenging problems in molecular evolution. The genetic code is an important universal feature of extant organisms and indicates a common ancestry of different forms of life on earth. Known variants of the genetic code can be mainly divided in mitochondrial and nuclear classes. Here we provide a new insight on the origin of the mitochondrial genetic code: we found that its degeneracy distribution can be explained by using a mathematical approach recently developed for the description of the Euplotes nuclear variant of the genetic code. The results point to a primeval mitochondrial genetic code composed of four base codons, which we call tesserae, that, among other features, exhibit outstanding error detection capabilities. The theoretical description suggests also a formulation of a plausible biological theory about the origin of protein coding. Such theory is based on the symmetry properties of hypothetical primeval chemical adaptors between nucleic acids and amino acids (ancient tRNA’s). Our paper provides a unified mathematical framework for different hypotheses on the origin of genetic coding. Also, it contributes to revisit our present view about the evolutionary steps that led to extant genetic codes by giving a new first-principles perspective on the difficult problem of the origin of the genetic code, and consequently, on the origin of life on earth.

Highlights

If all present forms of life descend from a common ancestor, the characteristics of such ancestor need to be searched among universally shared traits of extant organisms, non-universal traits being the consequence of accumulated divergence through evolutionary times
In this paper we have shown that the global degeneracy distribution of the vertebrate mitochondrial genetic code can be described by a mathematical model based on number representation systems
The mathematical approach allows the uncovering of many different symmetries and antisymmetries of the genetic code that seems strongly related to the organization of genetic information

Summary

G GUA Val GCA Ala GAA Glu GGA Gly A

In the case of the mitochondrial code, the degeneracy is explicitly determined by the two first digits of the non-power representation. The hypothesis included the idea that two independent groups of di-nucleotides were at the origin of the genetic code: the so called prefix and suffix doublets (Wu et al, 2005) Another recent work that emphasizes the role of dinucleotides put the attention on primeval symmetries of dinucleotides, in particular, the possibility that ancient tRNAs were reversible and, able to read a dinucleotide in both directions (Wilheim, 2004). - complementary (reading a codon in the complementary strand in the reverse 5’-3’ direction) These symmetries themselves allow for coding amino acids with some degeneracy. The second solution implies the presence of an independent anticodon in the tRNA molecule whose sequence coincides with the codon (tessera), i.e. the anti-(anti-codon) Another possibility allows the implementation of the reverse-complementary symmetry without further assumptions on the tRNA primeval molecules: the reading of the complementary fibre of DNA. Any pair of reverse-complement codons can be read by the same reversible adaptor (degeneracy 2)

C A U GR GUACR

5) Conclusions