Differential Codon Adaptation between dsDNA and ssDNA Phages in Escherichia coli

Abstract

Because phages use their host translation machinery, their codon usage should evolve toward that of highly expressed host genes. We used two indices to measure codon adaptation of phages to their host, rRSCU (the correlation in relative synonymous codon usage [RSCU] between phages and their host) and Codon Adaptation Index (CAI) computed with highly expressed host genes as the reference set (because phage translation depends on host translation machinery). These indices used for this purpose are appropriate only when hosts exhibit little mutation bias, so only phages parasitizing Escherichia coli were included in the analysis. For double-stranded DNA (dsDNA) phages, both rRSCU and CAI decrease with increasing number of transfer RNA genes encoded by the phage genome. rRSCU is greater for dsDNA phages than for single-stranded DNA (ssDNA) phages, and the low rRSCU values are mainly due to poor concordance in RSCU values for Y-ending codons between ssDNA phages and the E. coli host, consistent with the predicted effect of C→T mutation bias in the ssDNA phages. Strong C→T mutation bias would improve codon adaptation in codon families (e.g., Gly) where U-ending codons are favored over C-ending codons (“U-friendly” codon families) by highly expressed host genes but decrease codon adaptation in other codon families where highly expressed host genes favor C-ending codons against U-ending codons (“U-hostile” codon families). It is remarkable that ssDNA phages with increasing C→T mutation bias also increased the usage of codons in the “U-friendly” codon families, thereby achieving CAI values almost as large as those of dsDNA phages. This represents a new type of codon adaptation.

Isolation and Characterization of a Shewanella Phage–Host System from the Gut of the Tunicate, Ciona intestinalis

“…The codon adaptation index (CAI), which is expected to increase upon phage–host coevolution, was higher between S. fidelis 3313 and the three phages examined (SFCi1 (0.753), VP16C (0.747), and VP16T (0.758)), than between Vibrio parahaemolyticus (RIMD 2210633) and those phages (SFCi1 (0.624), VP16C (0.607), and VP16T (0.604)). No tRNAs were detected in the SFCi1 phage genome that could independently influence the codon usage bias [62]. …”

Bacteriophage evolution differs by host, lifestyle and genome

“…communication with W. Pope). For phages of other host phyla, lifestyle data was compiled from two online resources, PHACTS 34 and ACLAME 35 , as well as previously compiled data for subsets of these phages 19 , 23 , 36 – 38 and as well as other various literature. Lifestyle data was thus curated for over 40% of the phages in this database, resulting in 452 lytic and 614 temperate phages, and predominantly from the host phyla Actinobacteria (562 phages), Firmicutes (131 phages), and Proteobacteria (362 phages).…”

A Major Controversy in Codon-Anticodon Adaptation Resolved by a New Codon Usage Index

“…, Akashi 1994 ; Moriyama and Powell 1997 ; Ran and Higgs 2012 ; Xia 1998 , 2008 ), which states that (1) protein production is rate limited by both translation initiation and elongation efficiency, (2) codon usage and tRNA anticodons coevolve to adapt to each other, resulting in increased production of correctly translated proteins, and (3) the increased elongation efficiency and accuracy represent the driving force for the highly expressed genes to acquire a high degree of codon-anticodon adaptation. These studies not only advanced our understanding of the joint effect of mutation and selection on codon usage ( Chithambaram et al 2014a , b ; Palidwor et al 2010 ) but also resulted in improved computational tools for characterizing codon usage and codon-anticodon adaptation ( Sun et al 2013 ; Xia 2007 ).…”