Within-Host Evolution of Staphylococcus aureus during Asymptomatic Carriage

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Golubchik, Tanya ^a   Batty, Elizabeth M ^a   Miller, Ruth R ^b,c   Farr, Helen ^b,c   Young, Bernadette C ^b   Larner Svensson, Hanna ^c,d   Fung, Rowena ^b,c   Godwin, Heather ^e   Knox, Kyle ^a   Votintseva, Antonina ^b,c   Everitt, Richard G ^b   Street, Teresa ^a   Cule, Madeleine ^a   Ip, Camilla L C ^a   Didelot, Xavier ^a   Peto, Timothy E A ^b,c   Harding, Rosalind M ^a   Wilson, Daniel J ^b,d   Crook, Derrick W ^b,c   Bowden, Rory ^a,c,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; BACTERIOPHAGE; CONTROLLED STUDY; EVOLUTION; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; HOST PATHOGEN INTERACTION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL DIVERSITY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POINT MUTATION; POPULATION DYNAMICS; POPULATION GENETICS; SEQUENCE HOMOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; ASYMPTOMATIC INFECTIONS; CARRIER STATE; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HUMANS; INDEL MUTATION; NOSE; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84877034258     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061319     Document Type: Article

References (81)

1. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, et al. (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5: 751-762.
2. World Health Organization (2008) The Global Burden of Disease: 2004 Update. Available: http://www.who.int/healthinfo/global_burden_disease. Accessed 2012 April 12.
3. World Health Organization (2011) World Health Organization Mortality Database, ICD-10. 24 November 2011 update. Available: http://www.who.int/whosis/mort/download/en/index.html. Accessed 2012 April 12.
4. Moxon ER, Jansen VAA, (2005) Phage variation: understanding the behaviour of an accidental pathogen. Trends Microbiol 13: 563-565.
5. Nandi T, Ong C, Singh AP, Boddey J, Atkins T, et al. (2010) A Genomic Survey of Positive Selection in Burkholderia pseudomallei Provides Insights into the Evolution of Accidental Virulence. PLoS Pathog 6: e1000845.
6. Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L, et al. (2002) Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70: 4987-4996.
7. Chambers HF, Deleo FR, (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: 629-641.
8. Cordova SP, Heath CH, McGechie DB, Keil AD, Beers MY, et al. (2004) Methicillin-resistant Staphylococcus aureus bacteraemia in Western Australian teaching hospitals, 1997-1999: risk factors, outcomes and implications for management. J Hosp Infect 56: 22-28.
9. Tacconelli E, Venkataraman L, De Girolami PC, D'Agata EMC, (2004) Methicillin-resistant Staphylococcus aureus bacteraemia diagnosed at hospital admission: distinguishing between community-acquired versus healthcare-associated strains. J Antimicrob Chemother 53: 474-479.
10. Das I, O'Connell N, Lambert P, (2007) Epidemiology, clinical and laboratory characteristics of Staphylococcus aureus bacteraemia in a university hospital in UK. J Hosp Infect 65: 117-123.
11. Wyllie DH, Walker AS, Peto TE, Crook DW, (2007) Hospital exposure in a UK population, and its association with bacteraemia. J Hosp Infect 67: 301-307.
12. Ruimy R, Angebault C, Djossou F, Dupont C, Epelboin L, et al. (2010) Are host genetics the predominant determinant of persistent nasal Staphylococcus aureus carriage in humans? J Infect Dis 202: 924-934.
13. Melles DC, Gorkink RFJ, Boelens HAM, Snijders SV, Peeters JK, et al. (2004) Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J Clin Invest 114: 1732-1740.
14. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, et al. (2003) How clonal is Staphylococcus aureus? J Bacteriol 185: 3307-3316.
15. von Eiff C, Becker K, Machka K, Stammer H, Peters G, (2001) Nasal Carriage as a Source of Staphylococcus aureus Bacteremia. N Engl J Med 344: 11-16.
16. Pybus OG, Rambaut A, (2009) Evolutionary analysis of the dynamics of viral infectious disease. Nat Rev Genet 10: 540-550.
17. Drake JW, Charlesworth B, Charlesworth D, Crow JF, (1998) Rates of spontaneous mutation. Genetics 148: 1667-1686.
18. Achtman M, (2008) Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62: 53-70.
19. Achtman M, (2012) Insights from genomic comparisons of genetically monomorphic bacterial pathogens. Phil Trans R Soc Lond B Biol Sci 367: 860-867.
20. Wilson DJ (2012) Insights from genomics into bacterial pathogen populations. PLoS Pathog, in press.
21. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103: 8487-8492.
22. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, et al. (2007) Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci U S A 104: 9451-9456.
23. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D, et al. (2010) Host imprints on bacterial genomes - rapid, divergent evolution in individual patients. PLoS Pathog 6: e1001078.
24. Morelli G, Didelot X, Kusecek B, Scharwz S, Bahlawane C, et al. (2010) Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 22: e1001036.
25. McAdam PR, Holmes A, Templeton KE, Fitzgerald JR, (2011) Adaptive evolution of Staphylococcus aureus during chronic endobronchial infection of a cystic fibrosis patient. PLoS ONE 6: e24301.
26. Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, et al. (2011) Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A 108: 5033-5038.
27. Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, et al. (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43: 482-486.
28. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, et al. (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43: 1275-1280.
29. Young BC, Golubchik T, Batty EM, Fung R, Larner-Svensson H, et al. (2012) Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc Natl Acad Sci U S A 109: 4550-4555.
30. Harmsen D, Claus H, Witte W, Rothganger J, Turnwald D, et al. (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41: 5442-5448.
31. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG, (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38: 1008-1015.
32. Schaeffer SW, Miller EL, (1993) Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics 135: 541-552.
33. Awadalla P, Eyre-Walker A, Smith JM, (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286: 2524-2525.
34. Meunier J, Eyre-Walker A, (2001) The correlation between linkage disequilibrium and distance: implications for recombination in hominid mitochondria. Mol Biol Evol 18: 2132-2135.
35. McVean G, Awadalla P, Fearnhead P, (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160: 1231-1241.
36. Wilson DJ, McVean G, (2006) Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172: 1411-1425.
37. Hill WG, Robertson A, (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38: 226-231.
38. Hudson RR, Kaplan NL, (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
39. Holden MTG, Feil EJ, Lindsay JA, Peacock SJ, Day NPJ, et al. (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.
40. Didelot X, Falush D, (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251-1266.
41. Darling AE, Mau B, Perna NT, (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147.
42. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, et al. (2009) Reordering contigs of draft genomes using the Mauve Aligner. Bioinformatics 25: 2071-2073.
43. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
44. Kaneko J, Kimura T, Narita S, Tomita T, Kamio Y, (1998) Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215: 57-67.
45. Panton PN, Valentine FCO, (1932) Staphylococcal toxin. Lancet 1: 506-508.
46. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, et al. (2002) Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759.
47. De Haas CJ, Veldkamp KE, Peschel A, Weerkamp F, Van Wamel WJ, et al. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 199: 687-695.
48. Bae T, Baba T, Hiramatsu K, Schneewind O, (2006) Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62: 1035-1047.
49. Catchpole I, Thomas C, Davies A, Dyke KG, (1988) The nucleotide sequence of Staphylococcus aureus plasmid pT48 conferring inducible macrolide-lincosamide-streptogramin B resistance and comparison with similar plasmids expressing constitutive resistance. J Gen Microbiol 134: 697-709.
50. McDonald JH, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654.
51. Rocha EPC, Smith JM, Hurst LD, Holden MTG, Cooper JE, et al. (2006) Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239: 226-235.
52. Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, et al. (2011) Time-dependent rates of molecular evolution. Mol Ecol 20: 3087-3101.
53. Nicolaisen LA, Desai MM (2012) Distortions in gene genealogies due to purifying selection. Mol Biol Evol, in press.
54. Kluytmans J, van Belkum A, Verbrugh H, (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505-520.
55. VandenBergh MFQ, Yzerman EPF, van Belkum A, Boelens HAM, Sijmons M, et al. (1999) Follow-up of Staphylococcus aureus nasal carriage after 8 Years: redefining the persistent carrier state. J Clin Microbiol 37: 3133-3140.
56. Wright S, (1931) Evolution in Mendelian Populations. Genetics 16: 97-159.
57. Wertheim HF, Walsh E, Choudhurry R, Melles DC, Boelens HA, et al. (2008) Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med 5: e17.
58. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, et al. (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474.
59. Wakeley J, (2004) Metapopulation models for historical inference. Mol Ecol 13: 865-875.
60. Cespedes C, Said-Salim B, Miller M, Lo SH, Kreiswirth BN, et al. (2005) The clonality of Staphylococcus aureus nasal carriage. J Infect Dis 191: 444-452.
61. MacKinnon MM, Allen KD, (2000) Long-term MRSA carriage in hospital patients. J Hosp Infect 46: 216-221.
62. Vriens MR, Blok HE, Gigengack-Baars AC, Mascini EM, van der Werken C, et al. (2005) Methicillin-resistant Staphylococcus aureus carriage among patients after hospital discharge. Infect Control Hosp Epidemiol 26: 629-633.
63. Sanford MD, Widmer AF, Bale MJ, Jones RN, Wenzel RP, (1994) Efficient detection and long-term persistence of the carriage of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 19: 1123-1128.
64. Goerke C, Matias y Papenberg S, Dasbach S, Dietz K, Ziebach R, et al. (2004) Increased frequency of genomic alterations in Staphylococcus aureus during chronic infection is in part due to phage mobilization. J Infect Dis 189: 724-734.
65. Goerke C, Wirtz C, Flückiger U, Wolz C, (2006) Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection. Mol Microbiol 61: 1673-1685.
66. Goerke C, Gressingham M, Endler K, Breitkopf C, Wardecki K, et al. (2007) High phenotypic diversity in infecting but not in colonizing Staphylococcus aureus populations. Environ Microbiol 9: 3134-3142.
67. Griffiths RC, (2003) The frequency spectrum of a mutation, and its age, in a general diffusion model. Theor Popul Biol 64: 241-251.
68. Castillo-Ramírez S, Harris SR, Holden MTG, He M, Parkhill J, et al. (2011) The impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog 7: e1002129.
69. Eyre DW, Golubchik T, Gordon NC, Bowden R, Piazza P, et al. (2012) A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2: e001124.
70. Köser CU, Holden MTG, Ellington MJ, Cartwright EJP, Brown NM, et al. (2012) Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366: 2267-2275.
71. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
72. Chaudhuri RR, Loman NJ, Snyder LA, Bailey CM, Stekel DJ, et al. (2008) xBASE2: a comprehensive resource for comparative bacterial genomics. Nucleic Acids Res 36: D543-546.
73. Lunter G, Goodson M, (2011) Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21: 936-939.
74. Iqbal Z, Caccamo M, Turner I, Flicek P, McVean G, (2012) De novo assembly and genotyping of variants using colored de Bruijn graphs. Nat Genet 44: 226-232.
75. Didelot X, Eyre DW, Cule M, Ip CLC, Ansari A,et al. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Submitted, Genome Res.
76. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
77. Sokal RR, Rohlf FJ (1981) Biometry: the Principles and Practice of Statistics in Biological Research. New York: Freeman.
78. Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
79. Slatkin M, Hudson RR, (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555-562.
80. Hasegawa M, Kishino H, Yano T, (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Ecol 22: 160-174.
81. Stothard P, Wishart DS, (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21: 537-539.