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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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Schematics of preferred codon usage tables for E. coli, P. aeruginosa, and L. lactis following the conventions of Figure 4.Unlike E. coli, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%).
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pcbi-1000001-g006: Schematics of preferred codon usage tables for E. coli, P. aeruginosa, and L. lactis following the conventions of Figure 4.Unlike E. coli, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%).

Mentions: In this section we consider all sequenced phages that infect E. coli, Pseudomonas aeruginosa or Lactococcus lactis as their primary host. The latter two hosts were chosen because of they contain unusually extreme GC3 content: 88 %GC3 for P. aeurginosa and 25 %GC3 for L. lactis, genome-wide. The extreme GC3 content of these hosts give rise to opposing relationships between high CAI and GC3 – as indicated schematically in Figure 6. In particular, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%). Thus, these three hosts span a large spectrum of relationships between CAI and GC3. Since our randomization tests constrain amino acid and BCAI exactly (the ‘green’ test), and amino acids and GC3 exactly (the ‘orange’ test), we can control for any possible conflation between GC3 and CAI trends. Thus, the randomization tests are equally applicable to all of the phage genomes, regardless of their host.


Genome landscapes and bacteriophage codon usage.

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

Schematics of preferred codon usage tables for E. coli, P. aeruginosa, and L. lactis following the conventions of Figure 4.Unlike E. coli, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%).
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1000001-g006: Schematics of preferred codon usage tables for E. coli, P. aeruginosa, and L. lactis following the conventions of Figure 4.Unlike E. coli, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%).
Mentions: In this section we consider all sequenced phages that infect E. coli, Pseudomonas aeruginosa or Lactococcus lactis as their primary host. The latter two hosts were chosen because of they contain unusually extreme GC3 content: 88 %GC3 for P. aeurginosa and 25 %GC3 for L. lactis, genome-wide. The extreme GC3 content of these hosts give rise to opposing relationships between high CAI and GC3 – as indicated schematically in Figure 6. In particular, P. aeruginosa strongly favors GC3 in high-CAI codons (94%), and L. lactis strongly favors AT3 in high-CAI codons (72%). Thus, these three hosts span a large spectrum of relationships between CAI and GC3. Since our randomization tests constrain amino acid and BCAI exactly (the ‘green’ test), and amino acids and GC3 exactly (the ‘orange’ test), we can control for any possible conflation between GC3 and CAI trends. Thus, the randomization tests are equally applicable to all of the phage genomes, regardless of their host.

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