Elsevier

Biosystems

Volume 198, December 2020, 104239
Biosystems

LUCA as well as the ancestors of archaea, bacteria and eukaryotes were progenotes: Inference from the distribution and diversity of the reading mechanism of the AUA and AUG codons in the domains of life

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Highlights

  • If of a certain trait that exerts its function in some aspect of the genetic code, it is possible to identify the evolutionary stage of its origin then it would imply that this evolutionary moment would be characterized by a high translational noise.

  • I apply this rationale to the mechanism of modification of the base 34 of the anticodon of a tRNAIle that leads to the reading of AUA and AUG codons in archaea, bacteria and eukaryotes.

  • The phylogenetic distribution of this mechanism in these phyletic lines indicates that this mechanism originated at the stage of ancestors of these main phyletic lines, identifying them as progenotes.

Abstract

Here I use the rationale assuming that if of a certain trait that exerts its function in some aspect of the genetic code or, more generally, in protein synthesis, it is possible to identify the evolutionary stage of its origin then it would imply that this evolutionary moment would be characterized by a high translational noise because this trait would originate for the first time during that evolutionary stage. That is to say, if this trait had a non-marginal role in the realization of the genetic code, or in protein synthesis, then the origin of this trait would imply that, more generally, it was the genetic code itself that was still originating. But if the genetic code were still originating - at that precise evolutionary stage - then this would imply that there was a high translational noise which in turn would imply that it was in the presence of a protocell, i.e. a progenote that was by definition characterized by high translational noise. I apply this rationale to the mechanism of modification of the base 34 of the anticodon of an isoleucine tRNA that leads to the reading of AUA and AUG codons in archaea, bacteria and eukaryotes. The phylogenetic distribution of this mechanism in these phyletic lineages indicates that this mechanism originated only after the evolutionary stage of the last universal common ancestor (LUCA), namely, during the formation of cellular domains, i.e., at the stage of ancestors of these main phyletic lineages. Furthermore, given that this mechanism of modification of the base 34 of the anticodon of the isoleucine tRNA would result to emerge at a stage of the origin of the genetic code - despite in its terminal phases - then all this would imply that the ancestors of bacteria, archaea and eukaryotes were progenotes. If so, all the more so, the LUCA would also be a progenote since it preceded these ancestors temporally. A consequence of all this reasoning might be that since these three ancestors were of the progenotes that were different from each other, if at least one of them had evolved into at least two real and different cells - basically different from each other - then the number of cellular domains would not be three but it would be greater than three.

Section snippets

Introduction: choosing a character to determine the status of the universal ancestor and ancestors of major phyletic lineages

The nature of the last universal common ancestor (LUCA) i.e. the entity from which all organisms of the Earth would derive, has not yet been clarified. There are studies that indicate that it was a complete cell (genote) (Ouzounis and Kyrpides, 1996; Gogarten, 1995; Lazcano, 1995; Mushegian and Koonin, 1996; Ranea et al., 2006; Ouzounis et al., 2006; Delaye et al., 2002, 2005; Becerra et al., 2007; Mat et al., 2008; Tuller et al., 2010; Méheust et al., 2019). For example, although Méheust et

Materials and methods

To know how the agmatidine synthetase and lysidine synthetase are distributed in the main phyletic lineages, I used several search options available at the www.ncbi.nlm.nih.gov/site. In particular, I used - as a protein database - the Protein option and the logical operators AND, NOT, and OR and, for example, the terms BACTERIA, ARCHAEA, and EUKARYOTA to see which and how many organisms were in possession of these synthetases catalysing the reactions leading to agmatidine and lysidine.

Phylogenetic distribution of the modification of the position 34 of the anticodon in the tRNAIle leading to the evolution of lysidine in bacteria, agmatidine in archaea and inosine in eukaryotes

Reading the AUA codon is a difficult task for organisms because AUA codes for isoleucine (Ile) whereas AUG codes for methionine (Met) (Suzuki and Numata, 2014). This difficulty has been solved in archaea, bacteria and eukaryotes using completely independent but similar evolutionary strategies (Mandal et al., 2010; Suzuki and Numata, 2014). To read the AUA codon, archaea modify the base 34 of the anticodon of a tRNAIle to 2- agmatinylcytidine (agm2C or agmatidine), whereas the bacteria change

The different modifications of the base 34 of the anticodon of a tRNAIle in archaea, bacteria and eukaryotes identify the LUCA and the ancestors of these phyletic lineages as progenotes

The presence of different mechanisms for the recognition of AUA codon based on the evolution of lysidine in bacteria, agmatidine in archaea and inosine in eukaryotes (Muramatsu et al., 1988; Senger et al., 1997; Mandal et al., 2010; Suzuki and Numata, 2014; Nilsson and Alexander, 2019) would testify that these mechanisms emerged only after these phyletic lineages were separated. Otherwise, if they had emerged earlier, these mechanisms would be “identical” or at least not as dissimilar as they

The number of fundamental types of primary cells, i.e. the cellular domains of life, present on earth might be greater than three

The conclusion that LUCA as well as the ancestors of archaea, bacteria and eukaryotes were progenotes might have implications for the number of cellular domains, i.e. the number of basic types of primary cells present on our planet. In fact, if the ancestor of archaea, that of bacteria and that of eukaryotes had been different progenotes (Di Giulio, 2011, 2018), as corroborated here, then the real cells - and not protocells - would have appeared only after the stage of these ancestors. If at

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