A Comprehensive tRNA Genomic Survey Unravels the Evolutionary History of tRNA Arrays in Prokaryotes

Abstract

Considering the importance of tRNAs in the translation machinery, scant attention has been paid to tRNA array units defined as genomic regions containing at least 20 tRNA genes with a minimal tRNA gene density of two tRNA genes per kilobase. Our analysis of Acidithiobacillus ferrivorans CF27 and Acidithiobacillus ferrooxidans ATCC 23270T genomes showed that both display a tRNA array unit with syntenic conservation which mainly contributed to the tRNA gene redundancy in these two organisms. Our investigations into the occurrence and distribution of tRNA array units revealed that 1) this tRNA organization is limited to few phyla and mainly found in Gram-positive bacteria; and 2) the presence of tRNA arrays favors the redundancy of tRNA genes, in particular those encoding the core tRNA isoacceptors. Finally, comparative array organization revealed that tRNA arrays were acquired through horizontal gene transfer (from Firmicutes or unknown donor), before being subjected to tRNA rearrangements, deletions, and duplications. In Bacilli, the most parsimonious evolutionary history involved two common ancestors and the acquisition of their arrays arose late in evolution, in the genera branches. Functional roles of the array units in organism lifestyle, selective genetic advantage and translation efficiency, as well as the evolutionary advantages of organisms harboring them were proposed. Our study offers new insight into the structural organization and evolution of tRNA arrays in prokaryotic organisms.

Functionality of tRNAs encoded in a mobile genetic element from an acidophilic bacterium

“…An analysis of tRNA clusters in members of acidithiobacilli revealed that an array similar to that in ICEAfe1 is present in A. ferrivorans, another acidophilic bacterium belonging to the consortium of bioleaching microorganisms. Our phylogenetic data on the cluster of tRNA genes encoded in ICEAfe1 from A. ferrooxidans ATCC 23270 is consistent with the data presented by Tran et al 15 that includes the tRNA gene cluster from A. ferrivorans. Taken together, these data predict that these 2 arrays were acquired by HGT.…”

“…Although not all tRNA genes present in ICEAfe1 are encoded in this cluster, a similar synteny was found indicating probably a common origin. 15 A global analysis in the genus Acidithiobacilli revealed that codon usage of these 2 species is very similar (S6 Fig. 2), thus we believe that the effect on tAI of the cluster of tRNAs should also be similar in the 2 species.…”

“…14 A similar array of tRNA genes was found in Acidithiobacillus ferrivorans, a close relative to A. ferrooxidans. 15 We have previously demonstrated that a tRNA Glu encoded in ICEAfe1 from A. ferrooxidans is aminoacylated by the glutamyl-tRNA synthetase. 16 These observations raised the question as to what role these tRNA genes, clustered in a MGE, might play in A. ferrooxidans.…”

Exploring tRNA gene cluster in archaea

“…Besides mitogenomes, tRNA gene clusters have been shown to be abundant in Eukarya (Tawari et al, 2008;Bermudez-Santana et al, 2010). In prokaryotes, tRNA gene clusters were characterized in some bacteria, being prevalent in Firmicutes phylum and Mycobacterium genus (Tran et al, 2016;Morgado and Vicente, 2018), while in archaea, the presence of one tRNA gene cluster was only identified in the Methanobrevibacter M1 strain genome (Tran et al, 2016). Considering the common features among the three domains of life we hypothesized the prevalence of tRNA gene cluster also in archaea.…”

Operon-based approach for the inference of rRNA and tRNA evolutionary histories in bacteria

“…in bacteria are ribosomal RNA (rRNA) and transfer RNA (tRNA) operons [8,9]. There are several reasons for the interest in these operons, since those genes are fundamental for protein synthesis, and their numbers and organization can be used to better understand codon usage [10].…”