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Genome landscapes and bacteriophage codon usage.

Lucks JB, Nelson DR, Kudla GR, Plotkin JB - PLoS Comput. Biol. (2008)

Bottom Line: We find that 33 phage genomes exhibit highly non-random patterns in their GC3-content, use of host-preferred codons, or both.We show that the head and tail proteins of these phages exhibit significant bias towards host-preferred codons, relative to the non-structural phage proteins.Our results support the hypothesis of translational selection on viral genes for host-preferred codons, over a broad range of bacteriophages.

View Article: PubMed Central - PubMed

Affiliation: FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts, USA.

ABSTRACT
Across all kingdoms of biological life, protein-coding genes exhibit unequal usage of synonymous codons. Although alternative theories abound, translational selection has been accepted as an important mechanism that shapes the patterns of codon usage in prokaryotes and simple eukaryotes. Here we analyze patterns of codon usage across 74 diverse bacteriophages that infect E. coli, P. aeruginosa, and L. lactis as their primary host. We use the concept of a "genome landscape," which helps reveal non-trivial, long-range patterns in codon usage across a genome. We develop a series of randomization tests that allow us to interrogate the significance of one aspect of codon usage, such as GC content, while controlling for another aspect, such as adaptation to host-preferred codons. We find that 33 phage genomes exhibit highly non-random patterns in their GC3-content, use of host-preferred codons, or both. We show that the head and tail proteins of these phages exhibit significant bias towards host-preferred codons, relative to the non-structural phage proteins. Our results support the hypothesis of translational selection on viral genes for host-preferred codons, over a broad range of bacteriophages.

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Green (left) and orange (right) randomization tests for several phages.Bacteriophages P2 (A) and T3 (B) both infect E. coli. Phage D3112 (C) infects P. aeruginosa. Phage bIL286 (D) infects L. lactis. T3 is the only non-temperate phage of this group. See Table 2 for combined Fisher p-values for these tests. In the case of bIL286, note the lack of evidence for codon bias evident in the green and orange tests for bIL286, as confirmed by the insignificant p-values in Table 2. In this case, we cannot rule out the possibility that the observed pattern in GC3 is determined completely by the amino acid and CAI sequence (green), or that the observed pattern in CAI is determined by the amino acid and GC3 sequence (orange).
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pcbi-1000001-g007: Green (left) and orange (right) randomization tests for several phages.Bacteriophages P2 (A) and T3 (B) both infect E. coli. Phage D3112 (C) infects P. aeruginosa. Phage bIL286 (D) infects L. lactis. T3 is the only non-temperate phage of this group. See Table 2 for combined Fisher p-values for these tests. In the case of bIL286, note the lack of evidence for codon bias evident in the green and orange tests for bIL286, as confirmed by the insignificant p-values in Table 2. In this case, we cannot rule out the possibility that the observed pattern in GC3 is determined completely by the amino acid and CAI sequence (green), or that the observed pattern in CAI is determined by the amino acid and GC3 sequence (orange).

Mentions: Figure 7 shows results of these tests for several example genomes. P2, a temperate phage, and T3, a non-temperate phage both infect E. coli and both pass the control tests and exhibit significant ‘orange’ and ‘green’ results, as does D3112, a temperate phage that infects P. aeruginosa. However, not all phages that pass the control test exhibit significant ‘orange’ and ‘green’ results – as evidenced by bIL286, a temperate phage infecting L. lactis.


Genome landscapes and bacteriophage codon usage.

Lucks JB, Nelson DR, Kudla GR, Plotkin JB - PLoS Comput. Biol. (2008)

Green (left) and orange (right) randomization tests for several phages.Bacteriophages P2 (A) and T3 (B) both infect E. coli. Phage D3112 (C) infects P. aeruginosa. Phage bIL286 (D) infects L. lactis. T3 is the only non-temperate phage of this group. See Table 2 for combined Fisher p-values for these tests. In the case of bIL286, note the lack of evidence for codon bias evident in the green and orange tests for bIL286, as confirmed by the insignificant p-values in Table 2. In this case, we cannot rule out the possibility that the observed pattern in GC3 is determined completely by the amino acid and CAI sequence (green), or that the observed pattern in CAI is determined by the amino acid and GC3 sequence (orange).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2266997&req=5

pcbi-1000001-g007: Green (left) and orange (right) randomization tests for several phages.Bacteriophages P2 (A) and T3 (B) both infect E. coli. Phage D3112 (C) infects P. aeruginosa. Phage bIL286 (D) infects L. lactis. T3 is the only non-temperate phage of this group. See Table 2 for combined Fisher p-values for these tests. In the case of bIL286, note the lack of evidence for codon bias evident in the green and orange tests for bIL286, as confirmed by the insignificant p-values in Table 2. In this case, we cannot rule out the possibility that the observed pattern in GC3 is determined completely by the amino acid and CAI sequence (green), or that the observed pattern in CAI is determined by the amino acid and GC3 sequence (orange).
Mentions: Figure 7 shows results of these tests for several example genomes. P2, a temperate phage, and T3, a non-temperate phage both infect E. coli and both pass the control tests and exhibit significant ‘orange’ and ‘green’ results, as does D3112, a temperate phage that infects P. aeruginosa. However, not all phages that pass the control test exhibit significant ‘orange’ and ‘green’ results – as evidenced by bIL286, a temperate phage infecting L. lactis.

Bottom Line: We find that 33 phage genomes exhibit highly non-random patterns in their GC3-content, use of host-preferred codons, or both.We show that the head and tail proteins of these phages exhibit significant bias towards host-preferred codons, relative to the non-structural phage proteins.Our results support the hypothesis of translational selection on viral genes for host-preferred codons, over a broad range of bacteriophages.

View Article: PubMed Central - PubMed

Affiliation: FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts, USA.

ABSTRACT
Across all kingdoms of biological life, protein-coding genes exhibit unequal usage of synonymous codons. Although alternative theories abound, translational selection has been accepted as an important mechanism that shapes the patterns of codon usage in prokaryotes and simple eukaryotes. Here we analyze patterns of codon usage across 74 diverse bacteriophages that infect E. coli, P. aeruginosa, and L. lactis as their primary host. We use the concept of a "genome landscape," which helps reveal non-trivial, long-range patterns in codon usage across a genome. We develop a series of randomization tests that allow us to interrogate the significance of one aspect of codon usage, such as GC content, while controlling for another aspect, such as adaptation to host-preferred codons. We find that 33 phage genomes exhibit highly non-random patterns in their GC3-content, use of host-preferred codons, or both. We show that the head and tail proteins of these phages exhibit significant bias towards host-preferred codons, relative to the non-structural phage proteins. Our results support the hypothesis of translational selection on viral genes for host-preferred codons, over a broad range of bacteriophages.

Show MeSH