Evolution of aminoacyl-tRNA synthetases - Analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal genetransfer events

Phylogenetic analysis of aminoacyl-tRNA synthetases (aaRSs) of all 20 speci ficities from completely sequenced bacterial, archaeal, and eukaryotic geno mes reveals a complex evolutionary picture. Detailed examination of the dom ain architecture of aaRSs using sequence profile searches delineated a netw ork of partially conserved domains that is even more elaborate than previou sly suspected. Several unexpected evolutionary connections were identified, including the apparent origin of the \beta-subunit of bacterial GlyRS from the HD superfamily of hydrolases, a domain shared by bacterial AspRS and t he B subunit of archaeal glutamyl-tRNA amidotransferases, and another previ ously undetected domain that is conserved in a subset of ThrRS, guanosine p olyphosphate hydrolases and synthetases, and a family of GTPases. Compariso n of domain architectures and multiple alignments resulted in the delineati on of synapomorphies-shared derived characters, such as extra domains or in serts-for most of the aaRSs specificities. These synapomorphies partition s ets of aaRSs with the same specificity into two or more distinct and appare ntly monophyletic groups. In conjunction with cluster analysis and a modifi cation of the midpoint-rooting procedure, this partitioning was used to inf er the likely root position in phylogenetic trees. The topologies of the re sulting rooted trees for most of the aaRSs specificities are compatible wit h the evolutionary "standard model" whereby the earliest radiation event se parated bacteria from the common ancestor of archaea and eukaryotes as oppo sed to the two other possible evolutionary scenarios for the three major di visions of life. For almost all aaRSs specificities, however, this simple s cheme is confounded by displacement of some of the bacterial aaRSs by their eukaryotic or, less frequently, archaeal counterparts. Displacement of anc estral eukaryotic aaRS genes by bacterial ones, presumably of mitochondrial origin, was observed for three aaRSs. In contrast, there was no convincing evidence of displacement of archaeal aaRSs by bacterial ones. Displacement of aaRS genes by eukaryotic counterparts is most common among parasitic an d symbiotic bacteria, particularly the spirochaetes, in which 10 of the 19 aaRSs seem to have been displaced by the respective eukaryotic genes and tw o by the archaeal counterpart. Unlike the primary radiation events between the three main divisions of life, that were readily traceable through the p hylogenetic analysis of aaRSs, no consistent large-scale bacterial phylogen y could be established. In part, this may be due to additional gene displac ement events among bacterial lineages. Argument is presented that, although lineage-specific gene loss might have contributed to the evolution of some of the aaRSs, this is not a viable alternative to horizontal gene transfer as the principal evolutionary phenomenon in this gene class.