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

Abstract

During the endosymbiotic evolution of mitochondria, the genes for aminoacyl-tRNA synthetases were transferred to the ancestral nucleus. A further reduction of mitochondrial function resulted in mitochondrion-related organisms (MRO) with a loss of the organelle genome. The fate of the now redundant ancestral mitochondrial aminoacyl-tRNA synthetase genes is uncertain. The derived protein sequence for arginyl-tRNA synthetase from thirty mitosomal organisms have been classified as originating from the ancestral nuclear or mitochondrial gene and compared to the identity element at position 20 of the cognate tRNA that distinguishes the two enzyme forms. The evolutionary choice between loss and retention of the ancestral mitochondrial gene for arginyl-tRNA synthetase reflects the coevolution of arginyl-tRNA synthetase and tRNA identity elements.

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

“…In contrast, the mitochondrial-type enzyme could recognize a tRNA Arg with any nucleotide at position 20, again in a subcellular-independent manner, as, for example, in Fungi. The validity of such universal identity elements has previously been confirmed (Igloi 2021 ) for the relatively restricted sample size of amitochondrial organisms (Makiuchi and Nozaki 2014 ). Whether it also applies to a much more complex system of multi-organelle species, possibly with multiple arginyl-tRNA synthetase genes, has been examined here.…”

“…A set of 404 derived protein sequences corresponding to one or more distinct arginyl-tRNA synthetase genes from 264 non-metazoan, non-fungal eukaryote species and covering 32 taxonomic groups in the National Center for Biotechnology Information (NCBI) taxonomic classification were assembled (Igloi 2022 ). 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 ).…”

“…In the simplest application, an examination of amitochondrial species revealed the single arginyl-tRNA synthetase encoded by the genome always corresponded to the identity elements found in the cytosolic tRNA Arg irrespective of whether the enzyme was of the cytosolic or mitochondrial class. It was proposed that in amitochondrial organisms the choice between loss and retention of one type of arginyl-tRNA synthetase depended on the nature of the nucleotide at position 20 of the cognate tRNA (Igloi 2021 ).…”

Aminoacyl-tRNA Synthetase Evolution within the Dynamic Tripartite Translation System of Plant Cells

“…Such changes in targeting or tRNA substrates represent potentially radical perturbations in aaRS function, and we hypothesize that they could result in positive selection and accelerated evolution in aaRS sequence for at least three different reasons. First, aaRSs evolving to charge new tRNA substrates may require changes to key regions involved in recognition of tRNA “identity elements” ( Giegé et al 1998 ; Igloi 2021 , 2022 ). Second, mitochondria differ from the cytosol in numerous respects (e.g., osmotic conditions) that could potentially affect protein folding and tRNA interactions and, thus, create selection for changes in protein sequence.…”

Aminoacyl-tRNA synthetase evolution within the dynamic tripartite translation system of plant cells

“…Such changes in targeting or tRNA substrates represent potentially radical perturbations in aaRS function, and we hypothesize that they could result in positive selection and accelerated evolution in aaRS sequence for at least three different reasons. First, aaRSs evolving to charge new tRNA substrates may require changes to key regions involved in recognition of tRNA "identity elements" (Giegé, et al 1998;Igloi 2021Igloi , 2022. Second, mitochondria differ from the cytosol in numerous respects (e.g., osmotic conditions) that could potentially affect protein folding and tRNA interactions and, thus, create selection for changes in protein sequence.…”