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

Abstract

The genome of the acidophilic, bioleaching bacterium Acidithiobacillus ferrooxidans, strain ATCC 23270, contains 95 predicted tRNA genes. Thirty-six of these genes (all 20 species) are clustered within an actively excising integrative-conjugative element (ICEAfe1). We speculated that these tRNA genes might have a role in adapting the bacterial tRNA pool to the codon usage of ICEAfe1 genes. To answer this question, we performed theoretical calculations of the global tRNA adaptation index to the entire A. ferrooxidans genome with and without the ICEAfe1 encoded tRNA genes. Based on these calculations, we observed that tRNAs encoded in ICEAfe1 negatively contribute to adapt the tRNA pool to the codon use in A. ferrooxidans. Although some of the tRNAs encoded in ICEAfe1 are functional in aminoacylation or protein synthesis, we found that they are expressed at low levels. These findings, along with the identification of a tRNA-like RNA encoded in the same cluster, led us to speculate that tRNA genes encoded in the mobile genetic element ICEAfe1 might have acquired mutations that would result in either inactivation or the acquisition of new functions.

Global In-Silico Scenario of tRNA Genes and Their Organization in Virus Genomes

“…Besides, some tRNA genes occurring in these viruses are organized in clusters comprising up to dozens of tRNA genes [ 2 , 4 , 11 , 12 , 13 , 14 , 15 , 16 ]. Interestingly, such tRNA gene organization is particularly common in mitochondrial genomes [ 17 , 18 , 19 ], but large clusters have been observed in the three domains of life ( Archaea , Bacteria and Eukarya ) [ 16 , 20 , 21 , 22 , 23 , 24 , 25 ]. Studies indicate that the presence of tRNA genes in virus genomes would be to compensate for differences in codon and/or amino acid usage between virus and hosts, favoring an efficient protein synthesis and/or expanding the host range [ 2 , 4 ].…”

Codon usage revisited: Lack of correlation between codon usage and the number of tRNA genes in enterobacteria

“…We have found previously a similar trend while analyzing codon usage and tRNA gene content of an integrative conjugative element present in the genome of the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans [15,21]. Nevertheless, recent reports have shown that most tRNAs in this mobile element are expressed at very low levels [22], questioning their ability to improve gene expression. If it is common that changes in tRNA gene copy numbers produce only small changes in tRNA levels, then we would expect these have minor effects on gene expression and, consequently, on the frequency of codon usage in most genes of the genome.…”

“…who have questioned the role of tRNA gene numbers in selection of codon bias, based on the absence of correlation between the number of tRNA genes and enrichment of C vs U ending codons in the case of 4 amino acids coded by two codons translated by a single tRNA isoacceptor [28]. Probable mechanisms allowing this stability in codon usage in organisms where tRNA gene numbers vary, are silencing of acquired tRNA genes as has been observed in A. ferrooxidans [22] or regulation of either transcription or stability of tRNAs which has also been observed under a limited number of experimental conditions [29,30]. Both mechanisms are expected to occur much faster than changes in codons usage, which would require a much larger number of mutations [31].…”

Transfer RNA function and evolution

“…Emerging evidence indicates a new role for tRNA genes in bacterial conjugation. Alamos et al found that the acidophilic bacterium Acidithiobacillus ferrooxidans encodes 36 of its 95 tRNAs in an integrative-conjugative genetic element [13]. Indeed, Castillo et al show that the integrases encoded in the conjugative element recognize the anticodon stem loop region in the tRNA gene for active and site-specific recombination [10].…”