Evolution of aminoacyl-tRNA synthetases - Analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal genetransfer events
Yi. Wolf et al., Evolution of aminoacyl-tRNA synthetases - Analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal genetransfer events, GENOME RES, 9(8), 1999, pp. 689-710
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.