Causes for the intriguing presence of tRNAs in phages - PubMed (original) (raw)
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.
Figures
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.
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.
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.
Similar articles
- Aeromonas phages encode tRNAs for their overused codons.
Prabhakaran R, Chithambaram S, Xia X. Prabhakaran R, et al. Int J Comput Biol Drug Des. 2014;7(2-3):168-82. doi: 10.1504/IJCBDD.2014.061645. Epub 2014 May 28. Int J Comput Biol Drug Des. 2014. PMID: 24878728 - Bioinformatic analysis of the Acinetobacter baumannii phage AB1 genome.
Li P, Chen B, Song Z, Song Y, Yang Y, Ma P, Wang H, Ying J, Ren P, Yang L, Gao G, Jin S, Bao Q, Yang H. Li P, et al. Gene. 2012 Oct 10;507(2):125-34. doi: 10.1016/j.gene.2012.07.029. Epub 2012 Jul 31. Gene. 2012. PMID: 22868206 - Coevolution of codon usage and tRNA genes leads to alternative stable states of biased codon usage.
Higgs PG, Ran W. Higgs PG, et al. Mol Biol Evol. 2008 Nov;25(11):2279-91. doi: 10.1093/molbev/msn173. Epub 2008 Aug 6. Mol Biol Evol. 2008. PMID: 18687657 - Viral tRNAs and tRNA-like structures.
Dreher TW. Dreher TW. Wiley Interdiscip Rev RNA. 2010 Nov-Dec;1(3):402-14. doi: 10.1002/wrna.42. Epub 2010 Sep 13. Wiley Interdiscip Rev RNA. 2010. PMID: 21956939 Review. - The Significance of Mutualistic Phages for Bacterial Ecology and Evolution.
Obeng N, Pratama AA, Elsas JDV. Obeng N, et al. Trends Microbiol. 2016 Jun;24(6):440-449. doi: 10.1016/j.tim.2015.12.009. Epub 2016 Jan 27. Trends Microbiol. 2016. PMID: 26826796 Review.
Cited by
- Isolation, characterization, and application of a novel Pseudomonas fluorescens phage vB_PF_Y1-MI in contaminated milk.
Xuan G, Liu X, Wang Y, Lin H, Jiang X, Wang J. Xuan G, et al. Mol Genet Genomics. 2024 Oct 12;299(1):97. doi: 10.1007/s00438-024-02179-6. Mol Genet Genomics. 2024. PMID: 39395039 - The phage anti-restriction induced system: new insights into bacterial immunity and bacteriophage escape strategies.
Zhong Y, Lauschke VM. Zhong Y, et al. Signal Transduct Target Ther. 2024 Oct 5;9(1):269. doi: 10.1038/s41392-024-01995-x. Signal Transduct Target Ther. 2024. PMID: 39369022 Free PMC article. Review. No abstract available. - Modern microbiology: Embracing complexity through integration across scales.
Eren AM, Banfield JF. Eren AM, et al. Cell. 2024 Sep 19;187(19):5151-5170. doi: 10.1016/j.cell.2024.08.028. Cell. 2024. PMID: 39303684 Review. - A novel lytic phage infecting MDR Salmonella enterica and its application as effective food biocontrol.
Jaglan AB, Verma R, Vashisth M, Virmani N, Bera BC, Vaid RK, Anand T. Jaglan AB, et al. Front Microbiol. 2024 Aug 15;15:1387830. doi: 10.3389/fmicb.2024.1387830. eCollection 2024. Front Microbiol. 2024. PMID: 39211316 Free PMC article. - Characterization and Anti-Biofilm Activity of Lytic Enterococcus Phage vB_Efs8_KEN04 against Clinical Isolates of Multidrug-Resistant Enterococcus faecalis in Kenya.
Soro O, Kigen C, Nyerere A, Gachoya M, Georges M, Odoyo E, Musila L. Soro O, et al. Viruses. 2024 Aug 9;16(8):1275. doi: 10.3390/v16081275. Viruses. 2024. PMID: 39205249 Free PMC article.
References
- Bailly-Bechet M., Danchin A., Iqbal M., Marsili M., Vergassola M., Danchin A., Iqbal M., Marsili M., Vergassola M., Iqbal M., Marsili M., Vergassola M., Marsili M., Vergassola M., Vergassola M. Codon usage domains over bacterial chromosomes. PLoS Comp. Biol. 2006;2:e37. doi: 10.1371/journal.pcbi.0020037. - DOI - PMC - PubMed
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources