The Origin of the Genetic Code: Matter of Metabolism or Physicochemical Determinism?

Abstract

In the research field on the origin of the genetic code two lines of thought are evident. The first puts at the core of the origin of the genetic code the physicochemical properties of amino acids (1967; Woese et al. 1966; Jungck 1978; Weber and Lacey 1978; Lacey and Mullins 1983; Di Giulio 1989a, b; Taylor and Coates 1989; Di Giulio 1996; Freeland and Hurst 1998; Lacey et al. 1992). Indeed, the physicochemical theory of the origin of the genetic code suggests that these properties have been the main selective pressure that determined the organisation of the genetic code (Sonneborn 1965; Woese et al. 1966; Fitch and Upper 1987; Di Giulio 1997). A prediction in part equivalent is also made by the stereochemical theory of the origin of the genetic code that maintains that interactions between codons or anticodons and amino acids have been the main forces that organised the genetic code (Woese 1967; Shimizu 1982; Szathmary 1993; Yarus 1998; Yarus et al. 2009). Therefore, also for the stereochemical hypothesis the physicochemical properties of amino acids were essential in organising the code. On the other hand, the second line of thought considers the metabolism and the biosynthetic relationships between amino acids as the main force that defined the evolutionary organisation of the genetic code (Wong 1975, 2005; Di Giulio 2008a), with the properties of amino acids having only a subsidiary role in this organisation (Wong 1980; Di Giulio 1989a). The current special issue of the Journal of Molecular Evolution, dedicated to the Evolution of the Genetic Code, presents four papers that summarise this field of study at the moment and bring some insight into these two lines of thought. Naturally, whether the physicochemical properties of amino acids would reflect the structure of proteins, that is to say their function, then this would not be incompatible with the coevolution theory of the genetic code, because the protein structure, by means of the physicochemical properties of amino acids, might have been the main selective pressure that determined the genetic code organisation. Obviously, this would also imply a correlation between the biosynthetic relationships of amino acids and their physicochemical properties, in addition to that with the structure of the genetic code, as some works seem to indicate (Di Giulio 1991, 1996). One of the works presented in this special issue by Francis (2013) is inclined to maintain a similar position. Indeed, the title of this paper is: ‘Evolution of the genetic code by incorporation of amino acids that improved or changed protein function’. Furthermore, Francis (2013) considers the hypothesis that very early on the genetic code used only codons of the GNC kind (Ikehara 2002; Trifonov 2004; Francis 2011), a code completely compatible also with the coevolution theory (Di Giulio 2008a). However, the observation that the properties of amino acids are mirrored in the genetic code organisation does not necessarily imply their determining role in the genetic code organisation, unless one does not validate that the level reached by the minimisation of physicochemical distances between amino acids in the genetic code structure is very elevated. This, at the moment, does not seem to be the case (Wong 1980; Di Giulio 1989a; Di Giulio et al. 1994; Di M. Di Giulio (&) Laboratory for Molecular Evolution, Institute of Genetics and Biophysics ‘Adriano Buzzati Traverso’, CNR, Via P. Castellino, 111, 80131 Naples, Napoli, Italy e-mail: massimo.digiulio@igb.cnr.it; digiulio@igb.cnr.it