An extension of the coevolution theory of the origin of the genetic code

Abstract

Background: The coevolution theory of the origin of the genetic code suggests that the genetic code is an imprint of the biosynthetic relationships between amino acids. However, this theory does not seem to attribute a role to the biosynthetic relationships between the earliest amino acids that evolved along the pathways of energetic metabolism. As a result, the coevolution theory is unable to clearly define the very earliest phases of genetic code origin. In order to remove this difficulty, I here suggest an extension of the coevolution theory that attributes a crucial role to the first amino acids that evolved along these biosynthetic pathways and to their biosynthetic relationships, even when defined by the non-amino acid molecules that are their precursors.

Results: It is re-observed that the first amino acids to evolve along these biosynthetic pathways are predominantly those codified by codons of the type GNN, and this observation is found to be statistically significant. Furthermore, the close biosynthetic relationships between the sibling amino acids Ala-Ser, Ser-Gly, Asp-Glu, and Ala-Val are not random in the genetic code table and reinforce the hypothesis that the biosynthetic relationships between these six amino acids played a crucial role in defining the very earliest phases of genetic code origin.

Conclusion: All this leads to the hypothesis that there existed a code, GNS, reflecting the biosynthetic relationships between these six amino acids which, as it defines the very earliest phases of genetic code origin, removes the main difficulty of the coevolution theory. Furthermore, it is here discussed how this code might have naturally led to the code codifying only for the domains of the codons of precursor amino acids, as predicted by the coevolution theory. Finally, the hypothesis here suggested also removes other problems of the coevolution theory, such as the existence for certain pairs of amino acids with an unclear biosynthetic relationship between the precursor and product amino acids and the collocation of Ala between the amino acids Val and Leu belonging to the pyruvate biosynthetic family, which the coevolution theory considered as belonging to different biosyntheses.

Reviewers: This article was reviewed by Rob Knight, Paul Higgs (nominated by Laura Landweber), and Eugene Koonin.

Figure 1

Biosynthetic relationships between amino acids, as defined by their biosyntheses and their relationships with the glycolytic pathway and the citric acid cycle. The figure was taken from Taylor and Coates [11] with a few modifications. The numbers indicate the biosynthetic steps. DAP = diaminopimelic pathway, aKG = alpha-ketoglutarate, OOA = oxalacetic acid, PEP = phosphoenolpyruvate, PGA = phosphoglycerate, R-P3 = 5-phosphoribosylpyrophosphate, Ru-5-P = ribulose-5-phosphate. The other abbreviations are standard.

Figure 2

Biosynthetic relationships between amino acids and their precursor non-amino acid molecules, as defined in a particular stage of the evolution of the biosynthetic pathways of amino acids. With the sole exception of proline, these are also the amino acids that first appear in a study on the temporal origin of the appearance of amino acids [54]. See Fig. 1 for further information.

Figure 3

This shows three stages of genetic code evolution. All the abbreviations are standard. See text for discussion.

Figure 4

This shows a stage of the evolution of the genetic code: the one in which the precursor amino acid codon domains are formed, as predicted by the coevolution theory[9]. See text for discussion.