Molecular evidence for the evolution of the eukaryotic mitochondrial arginyl‐tRNA synthetase from the prokaryotic suborder Cystobacterineae

Abstract

The evolutionary origin of the family of eukaryotic aminoacyl‐tRNA synthetases that are essential to all living organisms is a matter of debate. In order to shed molecular light on the ancient source of arginyl‐tRNA synthetase, a total of 1347 eukaryotic arginyl‐tRNA synthetase sequences were mined from databases and analyzed. Their multiple sequence alignment reveals a signature sequence that is characteristic of the nuclear‐encoded enzyme, which is imported into mitochondria. Using this molecular beacon, the origins of this gene can be traced to modern prokaryotes. In this way, a previous phylogenetic analysis linking Myxococcus to the emergence of the eukaryotic mitochondrial arginyl‐tRNA synthetase is supported by the unique existence of the molecular signature within the suborder Cystobacterineae that includes Myxococcus.

Evolutionary Adjustment of tRNA Identity Rules in Bacillariophyta for Recognition by an Aminoacyl-tRNA Synthetase Adds a Facet to the Origin of Diatoms

“…For non-metazoans, the elements distinguishing the forms were not as clear-cut as in the case of Eumetazoans. In particular the five amino acid-deletion in the characteristic mitochondrial 5∆MSTR motif (Igloi 2020a ) was not always present. Instead, the cytosolic KFKTR-like motif (corresponding to the conserved Class I aminoacyl-tRNA synthetase KMSK region (Sekine et al 2001 )) was frequently replaced by MSSR, or similar.…”

“…Such conserved divergence is found at several sites throughout the protein as in cluster-specific deletions (Panel A). The compilation also shows the nature of the 5∆MSTR motif found in yeast (position 408) and which is typical of nuclear-encoded mitochondrial arginyl-tRNA synthetases (Igloi 2020a ). It is evident that none of the Bacillariophyta enzymes correspond to this motif but, as indicated additionally by the N-terminal GDYQ feature both Sequences1 and 2 all fulfil the requirements to be of the cytosolic form.…”

“…Species possessing a mitosomal organelle have been discussed previously (Igloi 2021 ) and were not included. Sequences from individual taxonomic groups were visually inspected in order to classify them into the cytosolic or mitochondrial category (Online Resource 1) using the sequence features described previously (Igloi 2020a ) (Table 1 ). For non-metazoans, the elements distinguishing the forms were not as clear-cut as in the case of Eumetazoans.…”

“…Therefore, the identity elements documented for the S.cerevisiae arginyl-tRNA synthetase, and in particular, the indifference to the base at position 20 in tRNA, correspond to those found in mitochondrial tRNAs having canonical cloverleaf structures, as in Fungi. An alignment of derived amino acid sequences of arginyl-tRNA synthetases over a wide phylogenetic range has uncovered sequence domains specific to the nuclear-encoded cytosolic and to the nuclear-encoded mitochondrial arginyl-tRNA synthetases, respectively (Igloi 2020a ) which one can use to classify the ancestral source of the corresponding gene (Table 1 ). Using this classification and a knowledge of the corresponding identity elements (Aldinger et al 2012 ) it is possible to follow the co-evolutionary development of the macromolecules.…”

The Evolutionary Fate of Mitochondrial Aminoacyl-tRNA Synthetases in Amitochondrial Organisms

“…This motif is also found in some bacteria, including E. coli which relies on the tRNA-A20 recognition element and may be a relic of the ancestral prokaryotic host of the proto-endosymbiont. It is absent from the prokaryotic suborder Cystobacterineae from which the mitochondrial arginyl-tRNA synthetase has been derived (Igloi 2020a). The mitochondrial enzyme, on the other hand, has, when aligned with the cytoplasmic version a barely discernible GDYQ-like motif but a five-amino acid deletion followed by an MSTR-like sequence nearer the C terminus (referred to here as Δ5MSTR).…”