Genome architecture, GC3 content, codon usage, and predicted translational adaptation of Salmonella temperate and virulent phages
- 1ne Health Institute, School of Science and Technology, University of Georgia, Tbilisi, Georgia
Abstract
IntroductionSalmonella enterica phages are important drivers of bacterial evolution and potential tools for phage-based applications. However, differences in genome architecture, codon usage, and predicted translational adaptation between Salmonella temperate and virulent phages remain uncertain and need to be determined.MethodsThis study elucidates genome-wide and functional-module-specific molecular signatures across Salmonella phage lifestyles. We analyzed 41 temperate and 41 virulent Salmonella phage genomes comprising 7,759 protein-coding genes. Because lifestyle is a genome-level attribute, statistical inference employed equal-genome-weight comparisons, whole-genome permutations, genome-cluster bootstrapping, and sensitivity analyses.ResultsThe virulent phages exhibited greater broad-scale genomic disconnectedness (81.7% versus 74.0% of within-group genome pairs lacking significant BLAST similarity) and larger mean genomes (80,784 versus 44,433 bp). The temperate phages showed higher genome-average overall GC and GC3 content, with “virulent”-minus-“temperate” differences of −4.484 and −7.706 percentage points, respectively (both q = 0.00013). Conversely, the virulent phages exhibited higher genome-average Codon Adaptation Index (CAI-2; difference = +0.0131) and Index of Translation Elongation (ITE; +0.0321), with associations persisting after adjustment for the nucleotide composition and coding-sequence length. The genome-equal effective number of codons (Nc) difference was not significant (q = 0.383). Genome-equal PERMANOVA detected significant differentiation across the complete molecular dataset (R2 = 0.1518; q = 0.0001) and all five gene functional categories, with the greatest effects in the DNA repair/recombination, lysis-associated, and structural genes. Only regulatory genes showed significantly different genome-level multivariate dispersion. Genome-average PCA scores differed significantly along GC-associated PC1 and a second axis associated with CAI-2, ITE, and sequence size. GC-adjusted CAI-2 -ITE correlations remained positive across both phage lifestyles (ρ = 0.771 and 0.776), with genome-cluster bootstrap confidence intervals excluding zero. Genome-level relative synonymous codon usage analyses identified 23 of 59 codons with FDR-significant, large-effect differences. Principal findings persisted in functional-annotation and genome-relatedness sensitivity analyses.DiscussionCollectively, these results identify complementary compositional and predicted codon-adaptation signatures in the selected phage lifestyle groups, while taxonomic imbalance and the absence of direct translational measurements limit further interpretation.
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BibTeX
@article{taktakishvili2026genome,
title = {{Genome architecture, GC3 content, codon usage, and predicted translational adaptation of Salmonella temperate and virulent phages}},
author = {Ketevan Taktakishvili and Davit Janelidze and Ana Gamkrelidze and Saba Kobakhidze and Tinatin Elbakidze and Mamuka Kotetishvili},
journal = {Frontiers in Microbiology},
year = {2026},
month = nov,
doi = {10.3389/fmicb.2026.1927342},
url = {https://doi.org/10.3389/fmicb.2026.1927342},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Genome architecture, GC3 content, codon usage, and predicted translational adaptation of Salmonella temperate and virulent phages
AU - Ketevan Taktakishvili
AU - Davit Janelidze
AU - Ana Gamkrelidze
AU - Saba Kobakhidze
AU - Tinatin Elbakidze
AU - Mamuka Kotetishvili
PY - 2026
DA - 2026/11/05
JO - Frontiers in Microbiology
DO - 10.3389/fmicb.2026.1927342
UR - https://doi.org/10.3389/fmicb.2026.1927342
AB - IntroductionSalmonella enterica phages are important drivers of bacterial evolution and potential tools for phage-based applications. However, differences in genome architecture, codon usage, and predicted translational adaptation between Salmonella temperate and virulent phages remain uncertain and need to be determined.MethodsThis study elucidates genome-wide and functional-module-specific molecular signatures across Salmonella phage lifestyles. We analyzed 41 temperate and 41 virulent Salmonella phage genomes comprising 7,759 protein-coding genes. Because lifestyle is a genome-level attribute, statistical inference employed equal-genome-weight comparisons, whole-genome permutations, genome-cluster bootstrapping, and sensitivity analyses.ResultsThe virulent phages exhibited greater broad-scale genomic disconnectedness (81.7% versus 74.0% of within-group genome pairs lacking significant BLAST similarity) and larger mean genomes (80,784 versus 44,433 bp). The temperate phages showed higher genome-average overall GC and GC3 content, with “virulent”-minus-“temperate” differences of −4.484 and −7.706 percentage points, respectively (both q = 0.00013). Conversely, the virulent phages exhibited higher genome-average Codon Adaptation Index (CAI-2; difference = +0.0131) and Index of Translation Elongation (ITE; +0.0321), with associations persisting after adjustment for the nucleotide composition and coding-sequence length. The genome-equal effective number of codons (Nc) difference was not significant (q = 0.383). Genome-equal PERMANOVA detected significant differentiation across the complete molecular dataset (R2 = 0.1518; q = 0.0001) and all five gene functional categories, with the greatest effects in the DNA repair/recombination, lysis-associated, and structural genes. Only regulatory genes showed significantly different genome-level multivariate dispersion. Genome-average PCA scores differed significantly along GC-associated PC1 and a second axis associated with CAI-2, ITE, and sequence size. GC-adjusted CAI-2 -ITE correlations remained positive across both phage lifestyles (ρ = 0.771 and 0.776), with genome-cluster bootstrap confidence intervals excluding zero. Genome-level relative synonymous codon usage analyses identified 23 of 59 codons with FDR-significant, large-effect differences. Principal findings persisted in functional-annotation and genome-relatedness sensitivity analyses.DiscussionCollectively, these results identify complementary compositional and predicted codon-adaptation signatures in the selected phage lifestyle groups, while taxonomic imbalance and the absence of direct translational measurements limit further interpretation.
SN - 1664-302X
ER -