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Atypical AT Skew in Firmicute Genomes Results from Selection and Not from Mutation

By Catherine A. Charneski, Frank Honti, Josephine M. Bryant, Laurence D. Hurst and Edward J. Feil

Abstract

The second parity rule states that, if there is no bias in mutation or selection, then within each strand of DNA complementary bases are present at approximately equal frequencies. In bacteria, however, there is commonly an excess of G (over C) and, to a lesser extent, T (over A) in the replicatory leading strand. The low G+C Firmicutes, such as Staphylococcus aureus, are unusual in displaying an excess of A over T on the leading strand. As mutation has been established as a major force in the generation of such skews across various bacterial taxa, this anomaly has been assumed to reflect unusual mutation biases in Firmicute genomes. Here we show that this is not the case and that mutation bias does not explain the atypical AT skew seen in S. aureus. First, recently arisen intergenic SNPs predict the classical replication-derived equilibrium enrichment of T relative to A, contrary to what is observed. Second, sites predicted to be under weak purifying selection display only weak AT skew. Third, AT skew is primarily associated with largely non-synonymous first and second codon sites and is seen with respect to their sense direction, not which replicating strand they lie on. The atypical AT skew we show to be a consequence of the strong bias for genes to be co-oriented with the replicating fork, coupled with the selective avoidance of both stop codons and costly amino acids, which tend to have T-rich codons. That intergenic sequence has more A than T, while at mutational equilibrium a preponderance of T is expected, points to a possible further unresolved selective source of skew

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3174206
Provided by: PubMed Central

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Citations

  1. (2007). A new method for assessing the effect of replication on DNA base composition asymmetry.
  2. (2007). A robust species tree for the alphaproteobacteria.
  3. (2005). A study on the correlation of nucleotide skews and the positioning of the origin of replication: different modes of replication in bacterial species.
  4. (2002). Asymmetric directional mutation pressures in bacteria.
  5. (1996). Asymmetric substitution patterns in the two DNA strands of bacteria.
  6. (1999). Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms.
  7. (1998). Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes.
  8. (2006). Comparisons of dN/dS are time dependent for closely related bacterial genomes.
  9. (2005). Core Team
  10. (2003). Danchin A
  11. (1994). Effects of deletions in the uncA-uncG intergenic regions on expression of uncG, the gene for the gamma subunit of the Escherichia coli F1Fo-ATPase. Biochim Biophys Acta 1183: 499–503. AT Skew Due to Selection, Not Mutation PLoS Genetics |
  12. (2010). Evidence that mutation is universally biased towards AT in bacteria.
  13. (2010). Eyre-Walker A
  14. (2010). Genome sequence of a recently emerged, highly transmissible, multi-antibioticand antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW).
  15. (2008). Highthroughput sequencing provides insights into genome variation and evolution in Salmonella Typhi.
  16. (1999). How does replication-associated mutational pressure influence amino acid composition of proteins?
  17. (2009). Inferring population mutation rate and sequencing error rate using the SNP frequency spectrum in a sample of DNA sequences.
  18. (1997). Influence of genomic G+C content on average amino-acid composition of proteins from 59 bacterial species.
  19. (2010). Intergenic transposable elements are not randomly distributed in bacteria.
  20. (1995). Intrastrand parity rules of DNA base composition and usage biases of synonymous codons.
  21. (2002). Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes?
  22. Maxima sourceforge.net (2009) Maxima, a Computer Algebra System. Version
  23. (2009). Measuring the Rates of Spontaneous Mutation From Deep and Large-Scale Polymorphism Data.
  24. (2002). Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis.
  25. (2010). Operon structure of Staphylococcus aureus.
  26. (2006). Origin of replication in circular prokaryotic chromosomes.
  27. (2011). Phylogenetic trees of the phylum Actinobacteria.
  28. (2004). Phylogeny of Firmicutes with special reference to Mycoplasma (Mollicutes) as inferred from phosphoglycerate kinase amino acid sequence data.
  29. (2010). Phylogeny of gammaproteobacteria.
  30. (2006). Protein evolution: causes of trends in amino-acid gain and loss. Nature 442: E11–12. discussion E12.
  31. (2007). Quantitative determination of gene strand bias in prokaryotic genomes.
  32. (2007). Separating the effects of mutation and selection in producing DNA skew in bacterial chromosomes.
  33. (2006). Similar compositional biases are caused by very different mutational effects.
  34. (1997). Strand asymmetries in DNA evolution.
  35. (1998). Strand compositional asymmetry in bacterial and large viral genomes.
  36. (2008). Testing for neutrality in samples with sequencing errors.
  37. (1989). The Code Within the Codons.
  38. (2000). The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes.
  39. (2008). The Organization of the Bacterial Genome.
  40. (2009). The Temporal Dynamics of Slightly Deleterious Mutations
  41. (2008). Universal patterns of purifying selection at noncoding positions in bacteria.
  42. (2010). Update of the All-Species Living Tree Project based on 16S and 23S rRNA sequence analyses.
  43. (1999). Viari A
  44. (1988). When polymerases collide: replication and the transcriptional organization of the E. coli chromosome.