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Home / Equine Research Bank / PLoS One / Phylogenetic analysis of Staphylococcus aureus CC398 reveals...
PloS one2014; 9(2); e88083; doi: 10.1371/journal.pone.0088083

Phylogenetic analysis of Staphylococcus aureus CC398 reveals a sub-lineage epidemiologically associated with infections in horses.

Abstract: In the early 2000s, a particular MRSA clonal complex (CC398) was found mainly in pigs and pig farmers in Europe. Since then, CC398 has been detected among a wide variety of animal species worldwide. We investigated the population structure of CC398 through mutation discovery at 97 genetic housekeeping loci, which are distributed along the CC398 chromosome within 195 CC398 isolates, collected from various countries and host species, including humans. Most of the isolates in this collection were received from collaborating microbiologists, who had preserved them over years. We discovered 96 bi-allelic polymorphisms, and phylogenetic analyses revealed that an epidemic sub-clone within CC398 (dubbed 'clade (C)') has spread within and between equine hospitals, where it causes nosocomial infections in horses and colonises the personnel. While clade (C) was strongly associated with S. aureus from horses in veterinary-care settings (p = 2 × 10(-7)), it remained extremely rare among S. aureus isolates from human infections.
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Publication Date: 2014-02-04 PubMed ID: 24505386PubMed Central: PMC3913741DOI: 10.1371/journal.pone.0088083Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper investigates the genetic structure of a specific variant of Staphylococcus aureus (CC398) and identifies a sub-group associated with horse infections.

Study Background and Objective

  • The study was initiated to explore the population structure of a particular MRSA clonal complex named CC398. This variant was initially discovered in pigs and pig farmers in Europe during the early 2000s. However, it has since been identified in a range of different animal species around the world.
  • The research aimed to understand the diversity and spread of this variant by examining its genetic structure, particularly focusing on any potential sub-group specific to horses.

Methodology

  • To map out the genetic structure, the researchers conducted a mutation discovery study by analyzing 97 genetic housekeeping loci distributed across the CC398 chromosome.
  • The study worked with 195 CC398 isolates collected from various countries and host species, including humans. Most of these isolates were sourced from collaborating microbiologists, who preserved them over a period of time.

Findings

  • During the analysis, 96 bi-allelic polymorphisms were discovered. Bi-allelic polymorphisms are variations at a single genetic location where there are exactly two possible forms.
  • The phylogenetic analyses revealed the existence of a specific sub-clone within CC398, which is referred to as ‘clade (C)’ in the study. This sub-clone has spread within and between equine hospitals, where it not only causes infections in horses, but also colonizes the hospital staff.
  • The statistical association demonstrated a very strong correlation between clade (C) and S. aureus from horses in veterinary-care settings. Remarkably, the clade (C) remained rare among human cases of S. aureus infection.

Conclusion

  • This study identified a sub-lineage of the CC398 variant of Staphylococcus aureus that appears to be associated with infections in horses.
  • The results emphasize the need for effective infection control strategies within equine hospitals to protect both horses and hospital personnel from this specific strain of infection.

Cite This Article

APA
Abdelbary MM, Wittenberg A, Cuny C, Layer F, Kurt K, Wieler LH, Walther B, Skov R, Larsen J, Hasman H, Fitzgerald JR, Smith TC, Wagenaar JA, Pantosti A, Hallin M, Struelens MJ, Edwards G, Böse R, Nübel U, Witte W. (2014). Phylogenetic analysis of Staphylococcus aureus CC398 reveals a sub-lineage epidemiologically associated with infections in horses. PLoS One, 9(2), e88083. https://doi.org/10.1371/journal.pone.0088083

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 9
Issue: 2
Pages: e88083

Researcher Affiliations

Abdelbary, Mohamed M H
  • Robert Koch Institute, Wernigerode, Germany.
Wittenberg, Anne
  • Institute of Microbiology and Epizootics, Free University Berlin, Berlin, Germany.
Cuny, Christiane
  • Robert Koch Institute, Wernigerode, Germany.
Layer, Franziska
  • Robert Koch Institute, Wernigerode, Germany.
Kurt, Kevin
  • Robert Koch Institute, Wernigerode, Germany.
Wieler, Lothar H
  • Institute of Microbiology and Epizootics, Free University Berlin, Berlin, Germany.
Walther, Birgit
  • Institute of Microbiology and Epizootics, Free University Berlin, Berlin, Germany.
Skov, Robert
  • Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark.
Larsen, Jesper
  • Microbiology and Infection Control, Statens Serum Institut, Copenhagen, Denmark.
Hasman, Henrik
  • National Food Institute, Technical University of Denmark, Lyngby, Denmark.
Fitzgerald, J Ross
  • The Roslin Institute, University of Edinburgh, Edinburgh, United Kingdom.
Smith, Tara C
  • Department of Epidemiology, College of Public Health, the University of Iowa, Iowa City, Iowa, United States of America.
Wagenaar, J A
  • Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.
Pantosti, Annalisa
  • Istituto Superiore di Sanità, Rome, Italy.
Hallin, Marie
  • Centre National de Référence Staphylococcus aureus, Microbiology Department, Erasme University Hospital, Université Libre de Bruxelles, Brussels, Belgium.
Struelens, Marc J
  • European Centre for Disease Prevention and Control, Stockholm, Sweden.
Edwards, Giles
  • Department of Microbiology, Scottish MRSA Reference Laboratory (SMRSARL), Glasgow Royal Infirmary, Glasgow, United Kingdom.
Böse, R
  • Labor Dr. Böse GmbH, Harsum, Germany.
Nübel, Ulrich
  • Robert Koch Institute, Wernigerode, Germany.
Witte, Wolfgang
  • Robert Koch Institute, Wernigerode, Germany.

MeSH Terms

  • Animals
  • Genetic Loci / genetics
  • Horse Diseases / epidemiology
  • Horse Diseases / genetics
  • Horse Diseases / microbiology
  • Horses / microbiology
  • Hospitals, Animal
  • Humans
  • Phylogeny
  • Polymorphism, Genetic / genetics
  • Staphylococcal Infections / epidemiology
  • Staphylococcal Infections / genetics
  • Staphylococcal Infections / microbiology
  • Staphylococcus aureus / genetics

Grant Funding

  • BB/I013873/1 / Biotechnology and Biological Sciences Research Council

Conflict of Interest Statement

Competing Interests: One or more of the authors (R. Böse) are employed by a commercial company Labor Dr. Böse GmbH. This does not alter the authors\' adherence to all the PLOS ONE policies on sharing data and materials.

References

This article includes 79 references
  1. Lowy FD. Staphylococcus aureus infections.. N Engl J Med 339: 520–532.
    pubmed: 9709046
  2. Devriese LA, Van Damme LR, Fameree L. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases.. Zentralbl Veterinarmed B 19: 598–605.
    pubmed: 4486473
  3. Scott GM, Thomson R, Malone-Lee J, Ridgway GL. Cross-infection between animals and man: possible feline transmission of Staphylococcus aureus infection in humans?. J Hosp Infect 12: 29–34.
    pubmed: 2905371
  4. Cefai C, Ashurst S, Owens C. Human carriage of methicillin-resistant Staphylococcus aureus linked with pet dog.. Lancet 344: 539–540.
    pubmed: 7914628
  5. Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. Methicillin-resistant Staphylococcus aureus in pig farming.. Emerg Infect Dis 11: 1965–1966.
    pmc: PMC3367632pubmed: 16485492
  6. Witte W, Strommenger B, Stanek C, Cuny C. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe.. Emerg Infect Dis 13: 255–258.
    pmc: PMC2725865pubmed: 17479888
  7. Guardabassi L, Stegger M, Skov R. Retrospective detection of methicillin resistant and susceptible Staphylococcus aureus ST398 in Danish slaughter pigs.. Vet Microbiol 122: 384–386.
    pubmed: 17467199
  8. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers.. PLoS One 4: e4258.
    pmc: PMC2626282pubmed: 19145257
  9. Khanna T, Friendship R, Dewey C, Weese JS. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers.. Vet Microbiol 128: 298–303.
    pubmed: 18023542
  10. Pan A, Battisti A, Zoncada A, Bernieri F, Boldini M. Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy.. Emerg Infect Dis 15: 845–847.
    pmc: PMC2687035pubmed: 19402995
  11. Agerso Y, Hasman H, Cavaco LM, Pedersen K, Aarestrup FM. Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs.. Vet Microbiol 157: 246–250.
    pubmed: 22245403
  12. Nemati M, Hermans K, Lipinska U, Denis O, Deplano A. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398.. Antimicrob Agents Chemother 52: 3817–3819.
    pmc: PMC2565892pubmed: 18663024
  13. Cuny C, Friedrich A, Kozytska S, Layer F, Nübel U. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species.. Int J Med Microbiol 300: 109–117.
    pubmed: 20005777
  14. Kehrenberg C, Cuny C, Strommenger B, Schwarz S, Witte W. Methicillin-resistant and -susceptible Staphylococcus aureus strains of clonal lineages ST398 and ST9 from swine carry the multidrug resistance gene cfr.. Antimicrob Agents Chemother 53: 779–781.
    pmc: PMC2630595pubmed: 19047652
  15. Tavakol M, Olde Riekerink RG, Sampimon OC, Van Wamel WJ, Van Belkum A. Bovine-associated MRSA ST398 in the Netherlands.. Acta Vet Scand 54: 28.
    pmc: PMC3413592pubmed: 22549050
  16. Monecke S, Kuhnert P, Hotzel H, Slickers P, Ehricht R. Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle.. Vet Microbiol 125: 128–140.
    pubmed: 17614219
  17. Persoons D, Van Hoorebeke S, Hermans K, Butaye P, de Kruif A. Methicillin-resistant Staphylococcus aureus in poultry.. Emerg Infect Dis 15: 452–453.
    pmc: PMC2666289pubmed: 19239762
  18. Fessler AT, Olde Riekerink RG, Rothkamp A, Kadlec K, Sampimon OC. Characterization of methicillin-resistant Staphylococcus aureus CC398 obtained from humans and animals on dairy farms.. Vet Microbiol .
    pubmed: 22655975
  19. Fessler A, Scott C, Kadlec K, Ehricht R, Monecke S. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis.. J Antimicrob Chemother 65: 619–625.
    pubmed: 20164198
  20. Fessler AT, Kadlec K, Hassel M, Hauschild T, Eidam C. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany.. Appl Environ Microbiol 77: 7151–7157.
    pmc: PMC3194878pubmed: 21724898
  21. Cuny C, Nathaus R, Layer F, Strommenger B, Altmann D. Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs.. PLoS One 4: e6800.
    pmc: PMC2728842pubmed: 19710922
  22. van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans.. Emerg Infect Dis 14: 479–483.
    pmc: PMC2570802pubmed: 18325267
  23. Graveland H, Duim B, van Duijkeren E, Heederik D, Wagenaar JA. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans.. Int J Med Microbiol 301: 630–634.
    pubmed: 21983338
  24. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans.. Emerg Infect Dis 13: 1834–1839.
    pmc: PMC2876750pubmed: 18258032
  25. Van den Broek, Van Cleef BA, Haenen A, Broens EM, Van der Wolf PJ. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms.. Epidemiol Infect 137: 700–708.
    pubmed: 18947444
  26. Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties.. MBio 3.
    pmc: PMC3302565pubmed: 22375071
  27. van der Mee-Marquet N, Francois P, Domelier-Valentin AS, Coulomb F, Decreux C. Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France.. Clin Infect Dis 52: 152–153.
    pubmed: 21148535
  28. Price LB, Stegger M, Hasman H, Aziz M, Larsen J. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock.. MBio 3.
    pmc: PMC3280451pubmed: 22354957
  29. van de Giessen AW, van Santen-Verheuvel MG, Hengeveld PD, Bosch T, Broens EM. Occurrence of methicillin-resistant Staphylococcus aureus in rats living on pig farms.. Prev Vet Med 91: 270–273.
    pubmed: 19523703
  30. Vincze S, Stamm I, Monecke S, Kopp PA, Semmler T. Molecular analysis of human and canine Staphylococcus aureus strains reveals distinct extended-host-spectrum genotypes independent of their methicillin resistance.. Appl Environ Microbiol 79: 655–662.
    pmc: PMC3553761pubmed: 23160118
  31. Cuny C, Strommenger B, Witte W, Stanek C. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital.. Microb Drug Resist 14: 307–310.
    pubmed: 19025385
  32. Van den Eede A, Martens A, Lipinska U, Struelens M, Deplano A. High occurrence of methicillin-resistant Staphylococcus aureus ST398 in equine nasal samples.. Vet Microbiol 133: 138–144.
    pubmed: 18701224
  33. Loeffler A, Lloyd DH. Companion animals: a reservoir for methicillin-resistant Staphylococcus aureus in the community?. Epidemiol Infect 138: 595–605.
    pubmed: 20056014
  34. Loeffler A, Kearns AM, Ellington MJ, Smith LJ, Unt VE. First isolation of MRSA ST398 from UK animals: a new challenge for infection control teams?. J Hosp Infect 72: 269–271.
    pubmed: 19481297
  35. van Duijkeren E, Moleman M, Sloet van Oldruitenborgh-Oosterbaan MM, Multem J, Troelstra A. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks.. Vet Microbiol 141: 96–102.
    pubmed: 19740613
  36. Sieber S, Gerber V, Jandova V, Rossano A, Evison JM. Evolution of multidrug-resistant Staphylococcus aureus infections in horses and colonized personnel in an equine clinic between 2005 and 2010.. Microb Drug Resist 17: 471–478.
    pubmed: 21875361
  37. O'Mahony R, Abbott Y, Leonard FC, Markey BK, Quinn PJ. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland.. Vet Microbiol 109: 285–296.
    pubmed: 16026939
  38. Seguin JC, Walker RD, Caron JP, Kloos WE, George CG. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission.. J Clin Microbiol 37: 1459–1463.
    pmc: PMC84801pubmed: 10203505
  39. Weese JS. Methicillin-resistant Staphylococcus aureus in animals.. ILAR J 51: 233–244.
    pubmed: 21131724
  40. Weese JS. Methicillin-resistant Staphylococcus aureus: an emerging pathogen in small animals.. J Am Anim Hosp Assoc 41: 150–157.
    pubmed: 15870248
  41. Nübel U, Dordel J, Kurt K, Strommenger B, Westh H. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus.. PLoS Pathog 6: e1000855.
    pmc: PMC2851736pubmed: 20386717
  42. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK. Evolution of MRSA during hospital transmission and intercontinental spread.. Science 327: 469–474.
    pmc: PMC2821690pubmed: 20093474
  43. Parker J, Rambaut A, Pybus OG. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty.. Infect Genet Evol 8: 239–246.
    pubmed: 17921073
  44. Nübel U, Roumagnac P, Feldkamp M, Song JH, Ko KS. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus.. Proc Natl Acad Sci U S A 105: 14130–14135.
    pmc: PMC2544590pubmed: 18772392
  45. Robinson DA, Enright MC. Evolution of Staphylococcus aureus by large chromosomal replacements.. J Bacteriol 186: 1060–1064.
    pmc: PMC344219pubmed: 14762000
  46. Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.. Proc Natl Acad Sci U S A 106: 19545–19550.
    pmc: PMC2780746pubmed: 19884497
  47. Holden MT, Hsu LY, Kurt K, Weinert LA, Mather AE. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic.. Genome Res 23: 653–664.
    pmc: PMC3613582pubmed: 23299977
  48. Ellington MJ, Hope R, Livermore DM, Kearns AM, Henderson K. Decline of EMRSA-16 amongst methicillin-resistant Staphylococcus aureus causing bacteraemias in the UK between 2001 and 2007.. J Antimicrob Chemother 65: 446–448.
    pubmed: 20035019
  49. Amorim ML, Faria NA, Oliveira DC, Vasconcelos C, Cabeda JC. Changes in the clonal nature and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital.. J Clin Microbiol 45: 2881–2888.
    pmc: PMC2045296pubmed: 17626175
  50. Nulens E, Gould I, MacKenzie F, Deplano A, Cookson B. Staphylococcus aureus carriage among participants at the 13th European Congress of Clinical Microbiology and Infectious Diseases.. Eur J Clin Microbiol Infect Dis 24: 145–148.
    pubmed: 15660253
  51. Wulf MW, Sorum M, van Nes A, Skov R, Melchers WJ. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study.. Clin Microbiol Infect 14: 29–34.
    pubmed: 17986212
  52. Wulf M, van Nes A, Eikelenboom-Boskamp A, de Vries J, Melchers W. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students, the Netherlands.. Emerg Infect Dis 12: 1939–1941.
    pmc: PMC3291345pubmed: 17326948
  53. Hanselman BA, Kruth SA, Rousseau J, Low DE, Willey BM. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel.. Emerg Infect Dis 12: 1933–1938.
    pmc: PMC3291342pubmed: 17326947
  54. Moodley A, Nightingale EC, Stegger M, Nielsen SS, Skov RL. High risk for nasal carriage of methicillin-resistant Staphylococcus aureus among Danish veterinary practitioners.. Scand J Work Environ Health 34: 151–157.
    pubmed: 18470441
  55. Anderson ME, Lefebvre SL, Weese JS. Evaluation of prevalence and risk factors for methicillin-resistant Staphylococcus aureus colonization in veterinary personnel attending an international equine veterinary conference.. Vet Microbiol 129: 410–417.
    pubmed: 18187274
  56. Panchaud Y, Gerber V, Rossano A, Perreten V. Bacterial infections in horses: a retrospective study at the University Equine Clinic of Bern.. Schweiz Arch Tierheilkd 152: 176–182.
    pubmed: 20361396
  57. Weese JS, Lefebvre SL. Risk factors for methicillin-resistant Staphylococcus aureus colonization in horses admitted to a veterinary teaching hospital.. Can Vet J 48: 921–926.
    pmc: PMC1950112pubmed: 17966332
  58. Weese JS, Archambault M, Willey BM, Hearn P, Kreiswirth BN. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002.. Emerg Infect Dis 11: 430–435.
    pmc: PMC3298236pubmed: 15757559
  59. Weese JS, Caldwell F, Willey BM, Kreiswirth BN, McGeer A. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veterinary hospital.. Vet Microbiol 114: 160–164.
    pubmed: 16384660
  60. Porphyre T, Giotis ES, Lloyd DH, Stark KD. A Metapopulation Model to Assess the Capacity of Spread of Meticillin-Resistant Staphylococcus aureus ST398 in Humans.. PLoS One 7: e47504.
    pmc: PMC3480390pubmed: 23112817
  61. Li M, Du X, Villaruz AE, Diep BA, Wang D. MRSA epidemic linked to a quickly spreading colonization and virulence determinant.. Nat Med 18: 816–819.
    pmc: PMC3378817pubmed: 22522561
  62. McAdam PR, Templeton KE, Edwards GF, Holden MT, Feil EJ. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus.. Proc Natl Acad Sci U S A 109: 9107–9112.
    pmc: PMC3384211pubmed: 22586109
  63. Strommenger B, Bartels MD, Kurt K, Layer F, Rohde SM. Evolution of methicillin-resistant Staphylococcus aureus towards increasing resistance.. J Antimicrob Chemother .
    pubmed: 24150844
  64. Nübel U, Nitsche A, Layer F, Strommenger B, Witte W. Single-nucleotide polymorphism genotyping identifies a locally endemic clone of methicillin-resistant Staphylococcus aureus .. PLoS One 7: e32698.
    pmc: PMC3302872pubmed: 22427866
  65. Stegger M, Liu CM, Larsen J, Soldanova K, Aziz M. Rapid Differentiation between Livestock-Associated and Livestock-Independent Staphylococcus aureus CC398 Clades.. PLoS One 8: e79645.
    pmc: PMC3828327pubmed: 24244535
  66. Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM. Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA.. PLoS One 8: e63704.
    pmc: PMC3646818pubmed: 23667659
  67. Li S, Skov RL, Han X, Larsen AR, Larsen J. Novel types of staphylococcal cassette chromosome mec elements identified in clonal complex 398 methicillin-resistant Staphylococcus aureus strains.. Antimicrob Agents Chemother 55: 3046–3050.
    pmc: PMC3101438pubmed: 21422209
  68. McCarthy AJ, van Wamel W, Vandendriessche S, Larsen J, Denis O. Staphylococcus aureus CC398 clade associated with human-to-human transmission.. Appl Environ Microbiol 78: 8845–8848.
    pmc: PMC3502926pubmed: 23042163
  69. Hallin M, De Mendonca R, Denis O, Lefort A, El Garch F. Diversity of accessory genome of human and livestock-associated ST398 methicillin resistant Staphylococcus aureus strains.. Infect Genet Evol 11: 290–299.
    pubmed: 21145988
  70. Strommenger B, Braulke C, Heuck D, Schmidt C, Pasemann B. spa Typing of Staphylococcus aureus as a frontline tool in epidemiological typing.. J Clin Microbiol 46: 574–581.
    pmc: PMC2238071pubmed: 18032612
  71. Feil EJ. Small change: keeping pace with microevolution.. Nat Rev Microbiol 2: 483–495.
    pubmed: 15152204
  72. Kurt K, Rasigade JP, Laurent F, Goering RV, Zemlickova H. Subpopulations of Staphylococcus aureus clonal complex 121 are associated with distinct clinical entities.. PLoS One 8: e58155.
    pmc: PMC3591430pubmed: 23505464
  73. Roumagnac P, Weill FX, Dolecek C, Baker S, Brisse S. Evolutionary history of Salmonella Typhi.. Science 314: 1301–1304.
    pmc: PMC2652035pubmed: 17124322
  74. van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages.. J Bacteriol 188: 1310–1315.
    pmc: PMC1367213pubmed: 16452413
  75. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.. Syst Biol 59: 307–321.
    pubmed: 20525638
  76. Rozas J. DNA sequence polymorphism analysis using DnaSP.. Methods Mol Biol 537: 337–350.
    pubmed: 19378153
  77. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.. Bioinformatics 25: 1451–1452.
    pubmed: 19346325
  78. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods.. Bioinformatics 19: 2496–2497.
    pubmed: 14668244
  79. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees.. BMC Evol Biol 7: 214.
    pmc: PMC2247476pubmed: 17996036
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