Elsevier

Biosystems

Volume 196, October 2020, 104174
Biosystems

The phylogenetic distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase in the fundamental lineages would imply that the ancestor of archaea, that of eukaryotes and LUCA were progenotes

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Highlights

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    The function of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase might be linked to the origin of the genetic code.

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    If the evolutionary stage of the origin of these two enzymes could be unambiguously identified, then at that particular evolutionary stage the genetic code should still have been originating.

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    That particular evolutionary moment would be attributed to the evolutionary stage of the progenote.

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    I have analyzed the distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln aminodotrasferase.

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    Since the origin of these two enzymes can be related to the evolutionary stages of ancestors of archaea and eukaryotes, this would indicate these ancestors as progenotes.

Abstract

The function of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase might be related to the origin of the genetic code because, for example, glutaminyl-tRNA synthetase catalyses the fundamental reaction that makes the genetic code. If the evolutionary stage of the origin of these two enzymes could be unambiguously identified, then the genetic code should still have been originating at that particular evolutionary stage because the fundamental reaction that makes the code itself was still evidently evolving. This would result in that particular evolutionary moment being attributed to the evolutionary stage of the progenote because it would have a relationship between the genotype and the phenotype not yet fully realized because the genetic code was precisely still originating. I then analyzed the distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln aminodotrasferase in the main phyletic lineages. Since in some cases the origin of these two enzymes can be related to the evolutionary stages of ancestors of archaea and eukaryotes, this would indicate these ancestors as progenotes because at that evolutionary moment the genetic code was evidently still evolving, thus realizing the definition of progenote. The conclusion that the ancestor of archaea and that of eukaryotes were progenotes would imply that even the last universal common ancestor (LUCA) was a progenote because it appeared, on the tree of life, temporally before these ancestors.

Section snippets

Introduction and the main argument

The nature of the Last Universal Common Ancestor (LUCA) has not yet been resolved; that is to say, whether it was a complete cell (genote) or a protocell (progenote) has not yet been understood. There are studies which suggest that the LUCA was a 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),

The late origin of aminoacyl-tRNA synthetases would imply that the corresponding evolutionary stage belonged to a progenote

The late origin of ARSs, as predicted by the theory of coevolution, might imply that since the origin of the genetic code precisely in its late phase, of completion, it could have already abandoned the evolutionary stage characterized by a high translational noise, namely, having abandoned the stage of progenote. It seems to me, however, that this is not possible because the origin of ARSs, even if it occurred at a late stage of the origin of the genetic code, should have been characterized in

Materials and methods

To confirm or know how, for example, the glutaminyl-tRNA synthetase and glutamyl-tRNAGln amidotransferase are distributed in the main phyletic lineages, I used several of 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 this ARS or the amidotransferase subunits

The formation of Gln-tRNAGln and the indirect pathway of aminoacylation of the tRNAGln

The main prediction of the coevolution theory of the origin of the genetic code would be as follows. As this theory is based on biosynthetic relationships between amino acids (Wong, 1975; Di Giulio, 2008) and being biosynthetically related amino acids, linked by biosynthetic transformations occurring on tRNA-like molecules, then its main prediction would be to suggest that some biosynthetic transformations between amino acids can still occur on tRNA molecules (Di Giulio, 1997, 2008). That is

The distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase corroborate a status of the progenote for the evolutionary stage of ancestors of eukaryotes, archaea and consequently that of the LUCA

An analysis, using a total of 2588 genomes, found that GlnRS was absent in 62% of genomes of prokaryotes (Chaliotis et al., 2017). I confirm that in the proteomes of archaea present in the Protein database at the www.ncbi.nlm.nih.gov/site - and consistent with what Chaliotis et al. (2017) observed - only 17 species of archaea contain proteins referred to as glutamine-tRNA ligase that should be GlnRSs and are found to be present only in asgardarchaeota, DPANN and an euryarchaeon. This

The distribution of the asparaginyl-tRNA synthetase and Asp-tRNAAsn amidotransferase in the main lineages: no implications for the nature of ancestors of the domains of life

As noted for glutamine, asparagine has also the Asp-tRNAAsn- > Asn-tRNAAsn pathway (Curnow et al., 1996; Ibba et al., 1997). That is to say, the formation of the Asn-tRNAAsn is ensured in addition to the asparaginyl-tRNA synthetase (AsnRS) also by the existence of the indirect pathway of aminoacylation.

In eukaryotes the direct pathway of aminoacylation is as frequent as that of the direct route. Indeed, I note that in the Protein database there are 2847 items representing the Asp-tRNAAsn

Conclusions

It is immediate that if the ancestor of archaea and that of eukaryotes had been progenotes then even the LUCA would be a progenote simply because the LUCA temporally preceded these ancestors. These conclusions are in accordance with other observations (Di Giulio, 2001, 2011, 2014, 2018, 2020a, 2020b) that show, for example, that the ancestor of eukaryotes was a progenote given its close phylogenetic closeness with asgardarchaeota (Di Giulio, 2020a). However, even stronger evidence of the

Declaration of competing interest

I declare no conflict of interest.

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