The Impact of Recombination on dN/dS within Recently Emerged Bacterial Clones

English version České info

The development of next-generation sequencing platforms is set to reveal an unprecedented level of detail on short-term molecular evolutionary processes in bacteria. Here we re-analyse genome-wide single nucleotide polymorphism (SNP) datasets for recently emerged clones of methicillin resistant Staphylococcus aureus (MRSA) and Clostridium difficile. We note a highly significant enrichment of synonymous SNPs in those genes which have been affected by recombination, i.e. those genes on mobile elements designated “non-core” (in the case of S. aureus), or those core genes which have been affected by homologous replacements (S. aureus and C. difficile). This observation suggests that the previously documented decrease in dN/dS over time in bacteria applies not only to genomes of differing levels of divergence overall, but also to horizontally acquired genes of differing levels of divergence within a single genome. We also consider the role of increased drift acting on recently emerged, highly specialised clones, and the impact of recombination on selection at linked sites. This work has implications for a wide range of genomic analyses.

Vyšlo v časopise: The Impact of Recombination on dN/dS within Recently Emerged Bacterial Clones. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002129
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002129

Souhrn

Zdroje

1. MaidenMCBygravesJAFeilEMorelliGRussellJE 1998 Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95 3140 3145

2. EnrightMCDayNPDaviesCEPeacockSJSprattBG 2000 Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38 1008 1015

3. EnrightMCRobinsonDARandleGFeilEJGrundmannH 2002 The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99 7687 7692

4. CirlanMSaadMComanGBilalNEElbashierAM 2005 International spread of major clones of methicillin resistant Staphylococcus aureus: nosocomial endemicity of multi locus sequence type 239 in Saudi Arabia and Romania. Infect Genet Evol 5 335 339

5. KoKSLeeJYSuhJYOhWSPeckKR 2005 Distribution of major genotypes among methicillin-resistant Staphylococcus aureus clones in Asian countries. J Clin Microbiol 43 421 426

6. XuBLZhangGYeHFFeilEJChenGR 2009 Predominance of the Hungarian clone (ST 239-III) among hospital-acquired meticillin-resistant Staphylococcus aureus isolates recovered throughout mainland China. J Hosp Infect 71 245 255

7. FeilEJNickersonEKChantratitaNWuthiekanunVSrisomangP 2008 Rapid detection of the pandemic methicillin-resistant Staphylococcus aureus clone ST 239, a dominant strain in Asian hospitals. J Clin Microbiol 46 1520 1522

8. ChongtrakoolPItoTMaXXKondoYTrakulsomboonS 2006 Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 50 1001 1012

9. Aires de SousaMCrisostomoMISanchesISWuJSFuzhongJ 2003 Frequent recovery of a single clonal type of multidrug-resistant Staphylococcus aureus from patients in two hospitals in Taiwan and China. J Clin Microbiol 41 159 163

10. NeelaVGhasemzadeh MoghaddamHvan BelkumAHorst-KreftDMarianaNS 2010 First report on methicillin-resistant Staphylococcus aureus of Spa type T037, Sequence Type 239, SCCmec type III/IIIA in Malaysia. Eur J Clin Microbiol Infect Dis 29 115 117

11. EdgeworthJDYadegarfarGPathakSBatraRCockfieldJD 2007 An outbreak in an intensive care unit of a strain of methicillin-resistant Staphylococcus aureus sequence type 239 associated with an increased rate of vascular access device-related bacteremia. Clin Infect Dis 44 493 501

12. AmaralMMCoelhoLRFloresRPSouzaRRSilva-CarvalhoMC 2005 The predominant variant of the Brazilian epidemic clonal complex of methicillin-resistant Staphylococcus aureus has an enhanced ability to produce biofilm and to adhere to and invade airway epithelial cells. J Infect Dis 192 801 810

13. RobinsonDAEnrightMC 2004 Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186 1060 1064

14. 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

15. SmythDSMcDougalLKGranFWManoharanAEnrightMC 2010 Population structure of a hybrid clonal group of methicillin-resistant Staphylococcus aureus, ST239-MRSA-III. PLoS ONE 5 e8582

16. HarrisSRFeilEJHoldenMTQuailMANickersonEK 2010 Evolution of MRSA during hospital transmission and intercontinental spread. Science 327 469 474

17. CroucherNJHarrisSRFraserCQuailMABurtonJ 2011 Rapid pneumococcal evolution in response to clinical interventions. Science 331 430 434

18. HeMSebaihiaMLawleyTDStablerRADawsonLF 2010 Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A 107 7527 7532

19. DobrindtUHochhutBHentschelUHackerJ 2004 Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2 414 424

20. HackerJCarnielE 2001 Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2 376 381

21. HackerJBenderLOttMWingenderJLundB 1990 Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog 8 213 225

22. FeilEJ 2004 Small change: keeping pace with microevolution. Nat Rev Microbiol 2 483 495

23. HoldenMTFeilEJLindsayJAPeacockSJDayNP 2004 Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101 9786 9791

24. FeilEJCooperJEGrundmannHRobinsonDAEnrightMC 2003 How clonal is Staphylococcus aureus? J Bacteriol 185 3307 3316

25. LindsayJAHoldenMT 2004 Staphylococcus aureus: superbug, super genome? Trends Microbiol 12 378 385

26. KuhnGFrancioliPBlancDS 2006 Evidence for clonal evolution among highly polymorphic genes in methicillin-resistant Staphylococcus aureus. J Bacteriol 188 169 178

27. LindsayJAHoldenMT 2006 Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct Integr Genomics 6 186 201

28. LindsayJA 2010 Genomic variation and evolution of Staphylococcus aureus. Int J Med Microbiol 300 98 103

29. Caro-QuinteroARodriguez-CastanoGPKonstantinidisKT 2009 Genomic insights into the convergence and pathogenicity factors of Campylobacter jejuni and Campylobacter coli species. J Bacteriol 191 5824 5831

30. KwanTLiuJDuBowMGrosPPelletierJ 2005 The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci U S A 102 5174 5179

31. BabaTTakeuchiFKurodaMYuzawaHAokiK 2002 Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359 1819 1827

32. NovickRP 2003 Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49 93 105

33. ZouDKanekoJNaritaSKamioY 2000 Prophage, phiPV83-pro, carrying panton-valentine leukocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of phiPV83-pro, phiPVL, phi11, and other phages. Biosci Biotechnol Biochem 64 2631 2643

34. RochaEPSmithJMHurstLDHoldenMTCooperJE 2006 Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239 226 235

35. BalbiKJFeilEJ 2007 The rise and fall of deleterious mutation. Res Microbiol 158 779 786

36. BalbiKJRochaEPFeilEJ 2009 The temporal dynamics of slightly deleterious mutations in Escherichia coli and Shigella spp. Mol Biol Evol 26 345 355

37. LarssonPElfsmarkDSvenssonKWikstromPForsmanM 2009 Molecular evolutionary consequences of niche restriction in Francisella tularensis, a facultative intracellular pathogen. PLoS Pathog 5 e1000472

38. KryazhimskiySPlotkinJB 2008 The population genetics of dN/dS. PLoS Genet 4 e1000304

39. KlimanRMHeyJ 1993 Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10 1239 1258

40. WillifordAComeronJM 2010 Local effects of limited recombination: historical perspective and consequences for population estimates of adaptive evolution. J Hered 101 Suppl 1 S127 134

41. SmithJMHaighJ 1974 Hitch-Hiking Effect of a Favorable Gene. Genet Res 23 23 35

42. CharlesworthBMorganMTCharlesworthD 1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134 1289 1303

43. KahankovaJPantucekRGoerkeCRuzickovaVHolochovaP 2010 Multilocus PCR typing strategy for differentiation of Staphylococcus aureus siphoviruses reflecting their modular genome structure. Environ Microbiol 12 2527 2538

44. HusonDHBryantD 2006 Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23 254 267

45. BegunDJAquadroCF 1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356 519 520

46. NachmanMW 1997 Patterns of DNA variability at X-linked loci in Mus domesticus. Genetics 147 1303 1316

47. MaraisGMouchiroudDDuretL 2001 Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci U S A 98 5688 5692

48. BetancourtAJWelchJJCharlesworthB 2009 Reduced Effectiveness of Selection Caused by a Lack of Recombination. Curr Biol 19 655 660

49. CutterADPayseurBA 2003 Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol Biol Evol 20 665 673

50. PresgravesDC 2005 Recombination enhances protein adaptation in Drosophila melanogaster. Curr Biol 15 1651 1656

51. HellmannIEbersbergerIPtakSEPaaboSPrzeworskiM 2003 A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 72 1527 1535

52. McDonaldMDougallAHoltDHuygensFOppedisanoF 2006 Use of a single-nucleotide polymorphism genotyping system to demonstrate the unique epidemiology of methicillin-resistant Staphylococcus aureus in remote aboriginal communities. J Clin Microbiol 44 3720 3727

53. RuimyRArmand-LefevreLBarbierFRuppeECocojaruR 2009 Comparisons between geographically diverse samples of carried Staphylococcus aureus. J Bacteriol 191 5577 5583

54. RuimyRAngebaultCDjossouFDupontCEpelboinL 2010 Are host genetics the predominant determinant of persistent nasal Staphylococcus aureus carriage in humans? J Infect Dis 202 924 934

55. DiepBAGillSRChangRFPhanTHChenJH 2006 Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367 731 739

56. Garcia PelayoMCUplekarSKeniryAMendoza LopezPGarnierT 2009 A comprehensive survey of single nucleotide polymorphisms (SNPs) across Mycobacterium bovis strains and M. bovis BCG vaccine strains refines the genealogy and defines a minimal set of SNPs that separate virulent M. bovis strains and M. bovis BCG strains. Infect Immun 77 2230 2238

57. NovichkovPSWolfYIDubchakIKooninEV 2009 Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes. J Bacteriol 191 65 73

58. HughesALFriedmanRRivaillerPFrenchJO 2008 Synonymous and nonsynonymous polymorphisms versus divergences in bacterial genomes. Mol Biol Evol 25 2199 2209

59. HoltKEParkhillJMazzoniCJRoumagnacPWeillFX 2008 High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40 987 993

60. SmithNHGordonSVde la Rua-DomenechRClifton-HadleyRSHewinsonRG 2006 Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis. Nat Rev Microbiol 4 670 681

61. WertheimHFMellesDCVosMCvan LeeuwenWvan BelkumA 2005 The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5 751 762

62. HaldaneJBS 1932 The causes of evolution London Longman, Green & Co. Limited

63. ConceicaoTAires-de-SousaMFuziMTothAPasztiJ 2007 Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study. Clin Microbiol Infect 13 971 979

64. HsuLYLoomba-ChlebickaNKohYLTanTYKrishnanP 2007 Evolving EMRSA-15 epidemic in Singapore hospitals. J Med Microbiol 56 376 379

65. Aires-de-SousaMCorreiaBde LencastreH 2008 Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 46 2912 2917

66. van PasselMWMarriPROchmanH 2008 The emergence and fate of horizontally acquired genes in Escherichia coli. PLoS Comput Biol 4 e1000059

67. TouchonMHoedeCTenaillonOBarbeVBaeriswylS 2009 Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5 e1000344

68. LawrenceJGOchmanH 1998 Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 95 9413 9417

69. VishnoiAKryazhimskiySBazykinGAHannenhalliSPlotkinJB 2010 Young proteins experience more variable selection pressures than old proteins. Genome Res 20 1574 1581

70. MorelliGDidelotXKusecekBSchwarzSBahlawaneC 2010 Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 6 e1001036

71. RochaEPCFeilEJ 2010 Mutational Patterns Cannot Explain Genome Composition: Are There Any Neutral Sites in the Genomes of Bacteria? Plos Genetics 6 e1001104

72. HildebrandFMeyerAEyre-WalkerA 2010 Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6 e1001107

73. HershbergRPetrovDA 2010 Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6 e1001115

74. PosadaD 2008 jModelTest: phylogenetic model averaging. Mol Biol Evol 25 1253 1256

75. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797

76. RicePLongdenIBleasbyA 2000 EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16 276 277

77. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556