Evolution of the Glx-tRNA synthetase family: the glutaminyl enzyme as a case of horizontal gene transfer.

Abstract

An important step ensuring the fidelity in protein biosynthesis is the aminoacylation of tRNAs by aminoacyl-tRNA synthetases. The accuracy of this process rests on a family of 20 enzymes, one for each amino acid. One exception is the formation of Gln-tRNA(Gln) that can be accomplished by two different pathways: aminoacylation of tRNA(Gln) with Gln by glutaminyl-tRNA synthetase (GlnRS; EC 6.1.1.18) or transamidation of Glu from Glu-tRNA(Gln) mischarged by glutamyl-tRNA synthetase (GluRS; EC 6.1.1.17). The latter pathway is widespread among bacteria and organelles that, accordingly, lack GlnRS. However, some bacterial species, such as Escherichia coli, do possess a GlnRS activity, which is responsible for Gln-tRNA(Gln) formation. In the cytoplasm of eukaryotic cells, both GluRS and GlnRS activities can be detected. To gain more insight into the evolutionary relationship between GluRS and GlnRS enzyme species, we have now isolated and characterized a human cDNA encoding GlnRS. The deduced amino acid sequence shows a strong similarity with other known GlnRSs and with eukaryotic GluRSs. A molecular phylogenetic analysis was conducted on the 14 GlxRS (GluRS or GlnRS) sequences available to date. Our data suggest that bacterial GlnRS has a eukaryotic origin and was acquired by a mechanism of horizontal gene transfer.

Duplication and Quadruplication of Arabidopsis thaliana Cysteinyl- and Asparaginyl-tRNA Synthetase Genes of Organellar Origin

“…Because of their ancient history, well-understood role, and high degree of conservation, they have been natural choices for many phylogenetic studies (Brown and Doolittle 1995;DiazLazcoz et al 1998;Hashimoto et al 1998;Kim et al 1998;Nagel and Doolittle 1995;Shiba et al 1998;Taupin and Leberman 1999;Wolf et al 1999). Unfortunately (in some respects), it appears that the evolutionary history of aaRS genes has not always been straightforward, with several proposed examples of gene duplications, fusions, and gain by horizontal transfer (DiazLazcoz et al 1998;Doolittle and Handy 1998;Lamour et al 1994;Wolf et al 1999;Handy and Doolittle 1999). Prokaryotes contain a basic set of 18-20 aaRs, but eukaryotes have more, as they contain a second compartment (mitochondrial) capable of translation.…”

Aminoacyl-tRNAs: setting the limits of the genetic code

“…In contrast, GlnRS, generally held to be the most recently evolved aaRS, seems to have no obvious residual relationship to amino acid metabolism. Instead the simultaneous existence of both D-GluRS and ND-GluRS, as still observed in a few bacteria, would seem to facilitate the replacement of the indirect route of Gln-tRNA Gln synthesis by GlnRS (Salazar et al 2003;Skouloubris et al 2003), either by bacterial GluRS evolution or horizontal gene transfer from eukarya (Lamour et al 1994).…”

“…Genome analysis and biochemical data reveal in bacteria four different scenarios, all of which are based on the presence of different operational pathways for the formation of Gln-tRNA and/or Asn-tRNA (Fig. 3). (1) Organisms with AsnRS and GlnRS: Some ␥-proteobacteria (e.g., E. coli) acquired GlnRS from eukaryotes by horizontal gene transfer (Lamour et al 1994) and therefore produce Asn-tRNA and Gln-tRNA by direct acylation. (2) Organisms lacking AsnRS and GlnRS using Asp/GluAdT: A larger set of bacteria (e.g., Chlamydia trachomatis) lacks these two synthetases.…”

On the Evolution of the tRNA-Dependent Amidotransferases, GatCAB and GatDE

“…6,[26][27][28][29] Given GatCAB is present in both Archaea and Bacteria while GatDE is archaeal specific, it was speculated the AdT in LUCA was GatCAB with GatDE evolving later in early archaea. 30 To address this hypothesis and to gain a better understanding of the evolution of the two AdTs, we examined the phylogenetic relationship between the kinase subunits of the two AdTs (GatB and GatE).…”