Abstract:Embedded in the sequence of each transfer RNA are elements that promote specific interactions with its cognate aminoacyl tRNAsynthetase. Although many such "identity elements" are known, their detection is difficult since they rely on unique structural signatures and the combinatorial action of multiple elements spread throughout the tRNA molecule. Since the anticodon is often a major identity determinant itself, it is possible to switch between certain tRNA functional types by means of anticodon substitutions… Show more
“…One advantage to species with tRNA gene redundancy (and consequently high tRNA gene copy number) is that loss of one tRNA gene may have relatively little impact on the overall tRNA population in the cell for that particular tRNA functional isoacceptor. As a high redundancy of tRNA genes indeed facilitates tRNA anticodon mutation as previously suggested ( Rogers and Griffiths-Jones 2014 ), organisms with tRNA array units would be subjected to anticodon shifts. F ig .…”
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.
“…One advantage to species with tRNA gene redundancy (and consequently high tRNA gene copy number) is that loss of one tRNA gene may have relatively little impact on the overall tRNA population in the cell for that particular tRNA functional isoacceptor. As a high redundancy of tRNA genes indeed facilitates tRNA anticodon mutation as previously suggested ( Rogers and Griffiths-Jones 2014 ), organisms with tRNA array units would be subjected to anticodon shifts. F ig .…”
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.
“…To confirm our hypothesis that the changes in translation efficiencies resulted from the increased cellular demand for tRNA CCG , the tRNA which translates CGG, we decided to elevate the availability of this tRNA and examine the effect on the translation phenotype. We, and others, have recently shown that a mechanism to increase tRNA availability is a mutation in the anticodon that changes the codon specificity of the tRNA (30,31). We have shown that such anticodon-switching mutations can maintain the functionality of tRNA genes and are utilized by many species as an adaptive mechanism of the cellular tRNA pool.…”
Section: Proteome-wide Changes In Translation Efficiencies Are Allevimentioning
Although the genetic code is redundant, synonymous codons for the same amino acid are not used with equal frequencies in genomes, a phenomenon termed "codon usage bias." Previous studies have demonstrated that synonymous changes in a coding sequence can exert significant cis effects on the gene's expression level. However, whether the codon composition of a gene can also affect the translation efficiency of other genes has not been thoroughly explored. To study how codon usage bias influences the cellular economy of translation, we massively converted abundant codons to their rare synonymous counterpart in several highly expressed genes in Escherichia coli. This perturbation reduces both the cellular fitness and the translation efficiency of genes that have high initiation rates and are naturally enriched with the manipulated codon, in agreement with theoretical predictions. Interestingly, we could alleviate the observed phenotypes by increasing the supply of the tRNA for the highly demanded codon, thus demonstrating that the codon usage of highly expressed genes was selected in evolution to maintain the efficiency of global protein translation. codon usage evolution | tRNA | codon-to-tRNA balance | translation efficiency | genome engineering S ince there are 61 sense codons but only 20 amino acids, most amino acids are encoded by more than a single codon. However, synonymous codons for the same amino acid are not utilized to the same extent across different genes or genomes. This phenomenon, termed "codon usage bias," has been the subject of intense research and was shown to affect gene expression and cellular function through varied processes in bacteria, yeast, and mammals (1-4).Although differential codon usage can result from neutral processes of mutational biases and drift (5-7), certain codon choices could be specifically favored as they increase the efficiency (8-12) or accuracy (13-17) of protein synthesis. These forces would typically lead to codon biases in a gene because they locally exert their effect on the gene in which the codons reside. Indeed, there is a positive correlation between a gene's expression level and the degree of its codon bias (1). Various systems have demonstrated how altering the codon usage synonymously can alter the expression levels of the manipulated genes (18-21), an effect that could reach more than 1,000-fold (22).In addition to such cis effects, it is possible that codon usage also acts in trans, namely, that the codon choice of some genes would affect the translation of others due to a "shared economy" of the entire translation apparatus (23-25). Previous theoretical works have suggested that an increase in the elongation rate may reduce the number of ribosomes on mRNAs and therefore may indirectly increase the rate of initiation of other transcripts due to an increase in the pool of free ribosomes (6,26). In addition, a recent computational study in yeast has also examined the indirect effects of synonymous codon changes on the translation of the entire transcriptome (2...
“…trnF-AAA has not been reported to be present in plant plastomes; however, it is an isoacceptor of trnF-GAA that is commonly found in plant plastomes, including those that are nonphotosynthetic. Mutations in anticodons (anticodon shifts) occurred many times in the evolution of several genomes, with isoacceptor shifts being more frequent than alloacceptor shifts ( Rogers and Griffiths-Jones 2014 ). The change of trnF-GAA to trnF-AAA may have been favorable, because ∼90% of all Phe codons in Epipogium are encoded by UUU.…”
The question on the patterns and limits of reduction of plastid genomes in nonphotosynthetic plants and the reasons of their conservation is one of the intriguing topics in plant genome evolution. Here, we report sequencing and analysis of plastid genome in nonphotosynthetic orchids Epipogium aphyllum and Epipogium roseum, which, with sizes of 31 and 19 kbp, respectively, represent the smallest plastid genomes characterized by now. Besides drastic reduction, which is expected, we found several unusual features of these “minimal” plastomes: Multiple rearrangements, highly biased nucleotide composition, and unprecedentedly high substitution rate. Only 27 and 29 genes remained intact in the plastomes of E. aphyllum and E. roseum—those encoding ribosomal components, transfer RNAs, and three additional housekeeping genes (infA, clpP, and accD). We found no signs of relaxed selection acting on these genes. We hypothesize that the main reason for retention of plastid genomes in Epipogium is the necessity to translate messenger RNAs (mRNAs) of accD and/or clpP proteins which are essential for cell metabolism. However, these genes are absent in plastomes of several plant species; their absence is compensated by the presence of a functional copy arisen by gene transfer from plastid to the nuclear genome. This suggests that there is no single set of plastid-encoded essential genes, but rather different sets for different species and that the retention of a gene in the plastome depends on the interaction between the nucleus and plastids.
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