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. 2007 Oct;17(10):1486-95.
doi: 10.1101/gr.6649807. Epub 2007 Sep 4.

Causes for the intriguing presence of tRNAs in phages

Marc Bailly-Bechet  1 , Massimo Vergassola, Eduardo Rocha
Affiliations

Causes for the intriguing presence of tRNAs in phages

Marc Bailly-Bechet et al. Genome Res. 2007 Oct.

Abstract

Phages have highly compact genomes with sizes reflecting their capacity to exploit the host resources. Here, we investigate the reasons for tRNAs being the only translation-associated genes frequently found in phages. We were able to unravel the selective processes shaping the tRNA distribution in phages by analyzing their genomes and those of their hosts. We found ample evidence against tRNAs being selected to facilitate phage integration in the prokaryotic chromosomes. Conversely, there is a significant association between tRNA distribution and codon usage. We support this observation by introducing a master equation model, where tRNAs are randomly gained from their hosts and then lost either neutrally or according to a set of different selection mechanisms. Those tRNAs present in phages tend to correspond to codons that are simultaneously highly used by the phage genes, while rare in the host genome. Accordingly, we propose that a selective recruitment of tRNAs compensates for the compositional differences between the phage and the host genomes. To further understand the importance of these results in phage biology, we analyzed the differences between temperate and virulent phages. Virulent phages contain more tRNAs than temperate ones, higher codon usage biases, and more important compositional differences with respect to the host genome. These differences are thus in perfect agreement with the results of our master equation model and further suggest that tRNA acquisition may contribute to higher virulence. Thus, even though phages use most of the cell's translation machinery, they can complement it with their own genetic information to attain higher fitness. These results suggest that similar selection pressures may act upon other cellular essential genes that are being found in the recently uncovered large viruses.

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Figures

Figure 1.
Figure 1.
Distribution of the number of tRNAs inside phage genomes. Empty bars stand for temperate phages, filled bars for virulent phages, and patterned bars for phage of unknown type. Note the heterogeneity of the counts and the tendency for virulent phages to have more tRNAs than temperate ones. Names are indicated for phages with 19 or more tRNAs in the form “(host species) Phage.”
Figure 2.
Figure 2.
Distribution of the frequencies of codon usage in phage genomes. The solid line is the distribution of codon frequencies; the dotted line, the distribution of codon frequencies, restricted to codons matching a tRNA on the considered phage genome. Note the peak around f = 0.03. The dash–dot line is the frequency distribution for all codons of all hosts. In the inset, the cumulated probability distribution (probability that a random tRNA will have a frequency superior or equal to the one given in abscissa) of the tail of the frequency distributions of the phages for all codons (solid line), and only the ones matching a tRNA (dotted line). Note the difference, indicating an excess of tRNAs matching high-frequency codons in phages.
Figure 3.
Figure 3.
Distribution of the frequencies of codon usage in virulent phage genomes (top) and temperate phage genomes (bottom). Light-gray filled bars, the distribution of codon frequencies, for all codons; black empty histogram bars, the distribution of codon frequencies, restricted to codons matching a tRNA on the considered phage genome. Note the difference between the distributions in both the virulent and the temperate case.
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