Causes for the intriguing presence of tRNAs in phages

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.

Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes

“…Although possibly true in some specific cases, this hypothesis cannot be generally true since phage integration does not always disrupt the tRNA gene and phages that integrate into a host's tRNA gene do not always bring in their own tRNA genes. 10 Moreover, this hypothesis does not explain the presence of more Figure 5. Relative frequency of codon usage for cluster A phages containing a specific tRNA gene (w/ tRNA), phages lacking that tRNA gene (w/o tRNA), for the capsid protein of phages with and without a specific tRNA gene (capsid w/ and capsid w/o), and for their potential hosts (see list in Fig.…”

“…[7][8] In addition, phages can encode their own tRNA genes, and the occasional presence of the tRNA genes has been called intriguing. [9][10] The complement of genes found in a phage is understood to represent a dynamic between gene acquisition via recombination events involving horizontal (or lateral) gene transfer from the genomes of their hosts and/or of co-infecting phages and retention through positive selection. [11][12] The prevalent hypothesis to explain the retention of tRNA genes proposes that these correspond to codons that are more common in the phage's genome than in the host's.…”

“…[11][12] The prevalent hypothesis to explain the retention of tRNA genes proposes that these correspond to codons that are more common in the phage's genome than in the host's. [9][10] This hypothesis makes at least 2 specific predictions: 1) phages that have codon usages similar to their hosts would not benefit from retaining any acquired tRNA genes and their genomes should not retain such genes (although they may contain genes or pseudogenes that have yet to be discarded); 2) phages with codon usages different from their hosts should retain tRNA genes that correspond to the codons more heavily used by the phage than its host. A corollary prediction is that lytic/virulent phages are more likely to retain tRNA genes they acquire since they do not integrate into the genome of their hosts and experience the mutational adaptations of temperate phages (changes in GC content to match that of their host).…”

“…This may explain why some virulent phages have more tRNA genes than temperate phages. 10 A related hypothesis proposes that it is amino acid usage, not codon usage, which leads to the retention of particular tRNA genes. The tRNA genes that are selected for retention are those that correspond to amino acids used by the phage more than its hosts.…”

Giant virus with a remarkable complement of genes infects marine zooplankton

“…These genes add to a rapidly growing number of virusencoded protein translation components. Some tRNA genes are scattered among bacteriophages and eukaryotic viruses such as the phycodnaviruses (17,18), and four tRNA synthetases along with several putative translation factors are found in Mimivirus (2). These findings imply that CroV and similarly complex viruses encode genes to modify and regulate the host translation system to their own advantage, which results in a "lifestyle" that is less dependent on host cell components than that of smaller viruses.…”