Atypical AT Skew in Firmicute Genomes Results from Selection and Not from Mutation
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.
Vyšlo v časopise:
Atypical AT Skew in Firmicute Genomes Results from Selection and Not from Mutation. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002283
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002283
Souhrn
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.
Zdroje
1. SueokaN 1995 Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. J Mol Evol 40 318 325
2. LobryJR 1996 Asymmetric substitution patterns in the two DNA strands of bacteria. Mol Biol Evol 13 660 665
3. LobryJRSueokaN 2002 Asymmetric directional mutation pressures in bacteria. Genome Biol 3 RESEARCH0058
4. RochaEPDanchinAViariA 1999 Universal replication biases in bacteria. Mol Microbiol 32 11 16
5. McLeanMJWolfeKHDevineKM 1998 Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J Mol Evol 47 691 696
6. FrankACLobryJR 1999 Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238 65 77
7. MrázekJKarlinS 1998 Strand compositional asymmetry in bacterial and large viral genomes. Proc Natl Acad Sci U S A 95 3720 3725
8. NikolaouCAlmirantisY 2005 A study on the correlation of nucleotide skews and the positioning of the origin of replication: different modes of replication in bacterial species. Nucleic Acids Res 33 6816 6822
9. TillierERCollinsRA 2000 The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes. J Mol Evol 50 249 257
10. FrancinoMPOchmanH 1997 Strand asymmetries in DNA evolution. Trends Genet 13 240 245
11. NecşuleaALobryJR 2007 A new method for assessing the effect of replication on DNA base composition asymmetry. Mol Biol Evol 24 2169 2179
12. RochaEPCTouchonMFeilEJ 2006 Similar compositional biases are caused by very different mutational effects. Genome Research 16 1537 1547
13. MortonRAMortonBR 2007 Separating the effects of mutation and selection in producing DNA skew in bacterial chromosomes. BMC Genomics 8 369
14. BrewerBJ 1988 When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53 679 686
15. RochaE 2002 Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes? Trends Microbiol 10 393 395
16. WorningPJensenLJHallinPFStaerfeldtHHUsseryDW 2006 Origin of replication in circular prokaryotic chromosomes. Environ Microbiol 8 353 361
17. HarrisSRFeilEJHoldenMTGQuailMANickersonEK 2010 Evolution of MRSA During Hospital Transmission and Intercontinental Spread. Science 327 469 474
18. RochaEPDanchinAViariA 1999 Translation in Bacillus subtilis: roles and trends of initiation and termination, insights from a genome analysis. Nucleic Acids Res 27 3567 3576
19. MolinaNvan NimwegenE 2008 Universal patterns of purifying selection at noncoding positions in bacteria. Genome Res 18 148 160
20. AngovEBrusilowWS 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
21. Castillo-RamírezSHarrisSHoldenMHeMParkhillJ 2011 The impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog 7 e1002129 doi:10.1371/journal.ppat.1002129
22. RochaEPSmithJMHurstLDHoldenMTCooperJE 2006 Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239 226 235
23. HershbergRPetrovDA 2010 Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6 e1001107 doi:10.1371/journal.pgen.1001107
24. HildebrandFMeyerAEyre-WalkerA 2010 Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6 e1001107 doi:10.1371/journal.pgen.1001107
25. MesserPW 2009 Measuring the Rates of Spontaneous Mutation From Deep and Large-Scale Polymorphism Data. Genetics 182 1219 1232
26. LiuXMaxwellTJBoerwinkleEFuYX 2009 Inferring population mutation rate and sequencing error rate using the SNP frequency spectrum in a sample of DNA sequences. Mol Biol Evol 26 1479 1490
27. AchazG 2008 Testing for neutrality in samples with sequencing errors. Genetics 179 1409 1424
28. TaylorFJRCoatesD 1989 The Code Within the Codons. Biosystems 22 177 187
29. HurstLDFeilEJRochaEP 2006 Protein evolution: causes of trends in amino-acid gain and loss. Nature 442 E11 12 discussion E12
30. AkashiHGojoboriT 2002 Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proceedings Of the National Academy Of Sciences Of the United States Of America 99 3695 3700
31. BartonMDDelneriDOliverSGRattrayMBergmanCM 2010 Evolutionary Systems Biology of Amino Acid Biosynthetic Cost in Yeast. PLoS ONE 5 e11935 doi:10.1371/journal.pone.0011935
32. WilliamsKPSobralBWDickermanAW 2007 A robust species tree for the alphaproteobacteria. J Bacteriol 189 4578 4586
33. YarzaPLudwigWEuzebyJAmannRSchleiferKH 2010 Update of the All-Species Living Tree Project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33 291 299
34. TakaiKSuzukiMNakagawaSMiyazakiMSuzukiY 2006 Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56 1725 1733
35. WilliamsKPGillespieJJSobralBWNordbergEKSnyderEE 2010 Phylogeny of gammaproteobacteria. J Bacteriol 192 2305 2314
36. LudwigWEuzébyJWhitmanWB 2011 Phylogenetic trees of the phylum Actinobacteria. GoodfellowMKämpferPHans-JürgenBTrujilloMESuzuki K-i Bergey's Manual of Systematic Bacteriology New York Springer
37. BalbiKJRochaEPCFeilEJ 2009 The Temporal Dynamics of Slightly Deleterious Mutations in Escherichia coli and Shigella spp. Molecular Biology and Evolution 26 345 355
38. RochaEPC 2008 The Organization of the Bacterial Genome. Annual Review of Genetics 42 211 233
39. RochaEPDanchinA 2003 Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 34 377 378
40. PlagueGR 2010 Intergenic transposable elements are not randomly distributed in bacteria. Genome Biol Evol 2 584 590
41. HoldenMTLindsayJACortonCQuailMACockfieldJD 2010 Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192 888 892
42. R Development Core Team 2005 R: A Language and Environment for Statistical Computing. Vienna, Austria R Foundation for Statistical Computing
43. ten Broeke-SmitsNJPronkTEJongeriusIBruningOWittinkFR 2010 Operon structure of Staphylococcus aureus. Nucleic Acids Res 38 3263 3274
44. Maxima sourceforge.net 2009 Maxima, a Computer Algebra System. Version 5.21.1. http://maxima.sourceforge.net
45. HoltKEParkhillJMazzoniCJRoumagnacPWeillFX 2008 High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nature Genetics 40 987 993
46. LobryJR 1997 Influence of genomic G+C content on average amino-acid composition of proteins from 59 bacterial species. Gene 205 309 316
47. MackiewiczPGierlikAKowalczukMDudekMRCebratS 1999 How does replication-associated mutational pressure influence amino acid composition of proteins? Genome Res 9 409 416
48. WolfMMullerTDandekarTPollackJD 2004 Phylogeny of Firmicutes with special reference to Mycoplasma (Mollicutes) as inferred from phosphoglycerate kinase amino acid sequence data. Int J Syst Evol Microbiol 54 871 875
49. de CarvalhoMOFerreiraHB 2007 Quantitative determination of gene strand bias in prokaryotic genomes. Genomics 90 733 740
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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