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Nucleotide composition affects codon usage toward the 3'-end.

ABSTRACT: The 3'-end of the coding sequence in several species is known to show specific codon usage bias. Several factors have been suggested to underlie this phenomenon, including selection against translation efficiency, selection for translation accuracy, and selection against RNA folding. All are supported by some evidence, but there is no general agreement as to which factors are the main determinants. Nor is it known how universal this phenomenon is, and whether the same factors explain it in different species. To answer these questions, we developed a measure that quantifies the codon usage bias at the gene end, and used it to compute this bias for 91 species that span the three domains of life. In addition, we characterized the codons in each species by features that allow discrimination between the different factors. Combining all these data, we were able to show that there is a universal trend to favor AT-rich codons toward the gene end. Moreover, we suggest that this trend is explained by avoidance from forming RNA secondary structures around the stop codon, which may interfere with normal translation termination.

SUBMITTER: Zahdeh F

PROVIDER: S-EPMC6892556 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Nucleotide composition affects codon usage toward the 3'-end.

Zahdeh Fouad F Carmel Liran L

PloS one 20191204 12

The 3'-end of the coding sequence in several species is known to show specific codon usage bias. Several factors have been suggested to underlie this phenomenon, including selection against translation efficiency, selection for translation accuracy, and selection against RNA folding. All are supported by some evidence, but there is no general agreement as to which factors are the main determinants. Nor is it known how universal this phenomenon is, and whether the same factors explain it in diffe ...[more]

PMID: 31800603

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Project description:The genetic material of the three domains of life (Bacteria, Archaea, and Eukaryota) is always double-stranded DNA, and their GC content (molar content of guanine plus cytosine) varies between ≈ 13% and ≈ 75%. Nucleotide composition is the simplest way of characterizing genomes. Despite this simplicity, it has several implications. Indeed, it is the main factor that determines, among other features, dinucleotide frequencies, repeated short DNA sequences, and codon and amino acid usage. Which forces drive this strong variation is still a matter of controversy. For rather obvious reasons, most of the studies concerning this huge variation and its consequences, have been done in free-living organisms. However, no recent comprehensive study of all known viruses has been done (that is, concerning all available sequences). Viruses, by far the most abundant biological entities on Earth, are the causative agents of many diseases. An overview of these entities is important also because their genetic material is not always double-stranded DNA: indeed, certain viruses have as genetic material single-stranded DNA, double-stranded RNA, single-stranded RNA, and/or retro-transcribing. Therefore, one may wonder if what we have learned about the evolution of GC content and its implications in prokaryotes and eukaryotes also applies to viruses. In this contribution, we attempt to describe compositional properties of ∼ 10,000 viral species: base composition (globally and according to Baltimore classification), correlations among non-coding regions and the three codon positions, and the relationship of the nucleotide frequencies and codon usage of viruses with the same feature of their hosts. This allowed us to determine how the base composition of phages strongly correlate with the value of their respective hosts, while eukaryotic viruses do not (with fungi and protists as exceptions). Finally, we discuss some of these results concerning codon usage: reinforcing previous results, we found that phages and hosts exhibit moderate to high correlations, while for eukaryotes and their viruses the correlations are weak or do not exist.

Project description:BACKGROUND: Despite the fact that the organization of the ciliate mitochondrial genome is exceptional, only few ciliate mitochondrial genomes have been sequenced until today. All ciliate mitochondrial genomes are linear. They are 40 kb to 47 kb long and contain some 50 tightly packed genes without introns. Earlier studies documented that the mitochondrial guanine + cytosine contents are very different between Paramecium tetraurelia and all studied Tetrahymena species. This raises the question of whether the high mitochondrial G+C content observed in P. tetraurelia is a characteristic property of Paramecium mtDNA, or whether it is an exception of the ciliate mitochondrial genomes known so far. To test this question, we determined the mitochondrial genome sequence of Paramecium caudatum and compared the gene content and sequence properties to the closely related P. tetraurelia. RESULTS: The guanine + cytosine content of the P. caudatum mitochondrial genome was significantly lower than that of P. tetraurelia (22.4% vs. 41.2%). This difference in the mitochondrial nucleotide composition was accompanied by significantly different codon usage patterns in both species, i.e. within P. caudatum clearly A/T ending codons dominated, whereas for P. tetraurelia the synonymous codons were more balanced with a higher number of G/C ending codons. Further analyses indicated that the nucleotide composition of most members of the genus Paramecium resembles that of P. caudatum and that the shift observed in P. tetraurelia is restricted to the P. aurelia species complex. CONCLUSIONS: Surprisingly, the codon usage bias in the P. caudatum mitochondrial genome, exemplified by the effective number of codons, is more similar to the distantly related T. pyriformis and other single-celled eukaryotes such as Chlamydomonas, than to the closely related P. tetraurelia. These differences in base composition and codon usage bias were, however, not reflected in the amino acid composition. Most probably, the observed picture is best explained by a hitherto unknown (neutral or adaptive) mechanism that increased the guanine + cytosine content in P. tetraurelia mtDNA on the one hand, and strong purifying selection on the ancestral amino acid composition on the other hand. These contradicting forces are counterbalanced by a considerably altered codon usage pattern.

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Nucleotide composition affects codon usage toward the 3'-end.

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Nucleotide composition affects codon usage toward the 3'-end.

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