Skip to main content
Log in

Staphylococcus aureus mobile genetic elements

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Among the bacteria groups, most of them are known to be beneficial to human being whereas only a minority is being recognized as harmful. The pathogenicity of bacteria is due, in part, to their rapid adaptation in the presence of selective pressures exerted by the human host. In addition, through their genomes, bacteria are subject to mutations, various rearrangements or horizontal gene transfer among and/or within bacterial species. Bacteria’s essential metabolic functions are generally encoding by the core genes. Apart of the core genes, there are several number of mobile genetic elements (MGE) acquired by horizontal gene transfer that might be beneficial under certain environmental conditions. These MGE namely bacteriophages, transposons, plasmids, and pathogenicity islands represent about 15 % Staphylococcus aureus genomes. The acquisition of most of the MGE is made by horizontal genomic islands (GEI), recognized as discrete DNA segments between closely related strains, transfer. The GEI contributes to the wide spread of microorganisms with an important effect on their genome plasticity and evolution. The GEI are also involve in the antibiotics resistance and virulence genes dissemination. In this review, we summarize the mobile genetic elements of S. aureus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Lindsay JA, Holden MT (2004) Staphylococcus aureus: superbug, super genome? Trends Microbiol 12(8):378–385. doi:10.1016/j.tim.2004.06.004

    CAS  PubMed  Google Scholar 

  2. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3(9):722–732. doi:10.1038/nrmicro1235

    CAS  PubMed  Google Scholar 

  3. Siefert JL (2009) Defining the mobilome. Methods Mol Biol 532:13–27. doi:10.1007/978-1-60327-853-9_2

    CAS  PubMed  Google Scholar 

  4. Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54:641–679. doi:10.1146/annurev.micro.54.1.641

    CAS  PubMed  Google Scholar 

  5. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, Flannagan SE, Kolonay JF, Shetty J, Killgore GE, Tenover FC (2003) Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302(5650):1569–1571. doi:10.1126/science.1090956

    CAS  PubMed  Google Scholar 

  6. Mlynarczyk A, Mlynarczyk G, Jeljaszewicz J (1998) The genome of Staphylococcus aureus: a review. Zentralblatt fur Bakteriologie 287(4):277–314

    CAS  PubMed  Google Scholar 

  7. Sharma VK, Johnston JL, Morton TM, Archer GL (1994) Transcriptional regulation by TrsN of conjugative transfer genes on staphylococcal plasmid pGO1. J Bacteriol 176(12):3445–3454

    PubMed Central  CAS  PubMed  Google Scholar 

  8. Goering RV, Teeman BA, Ruff EA (1985) Comparative physical and genetic maps of conjugal plasmids mediating aminoglycoside resistance in Staphylococcus aureus in the United States. In: Jeljaszewicz U (ed) The Staphylococci, vol Suppl. 14. Gustav Fischer Verlag, New York, pp 625–628

  9. Novick RP (1993) Staphylococcus. In: Sonenhein A, Hoch A, Losich R (eds) Biochemistry, physiology and molecular genetics: Bacillus subtilis and other gram positive bacteria. American Society for Microbiology, Washington, pp 17–33

    Google Scholar 

  10. Malachowa N, DeLeo FR (2010) Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 67(18):3057–3071. doi:10.1007/s00018-010-0389-4

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Lowy FD (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Investig 111(9):1265–1273. doi:10.1172/JCI18535

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Jeljaszewicz J, Mlynarczyk G, Mlynarczyk A (2000) Antibiotic resistance in Gram-positive cocci. Int J Antimicrob Agents 16(4):473–478

    CAS  PubMed  Google Scholar 

  13. Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7(9):629–641. doi:10.1038/nrmicro2200

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Kernodle DS (2000) Mechanisms of resistance to β-lactam antibiotics. In: Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (eds) Gram-positive pathogens. American Society for Microbiology, Washington, DC, pp 609–620

    Google Scholar 

  15. Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T, Tenover FC (1997) Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 40(1):135–136

    CAS  PubMed  Google Scholar 

  16. Showsh SA, De Boever EH, Clewell DB (2001) Vancomycin resistance plasmid in Enterococcus faecalis that encodes sensitivity to a sex pheromone also produced by Staphylococcus aureus. Antimicrob Agents Chemother 45(7):2177–2178

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Woodford N, Johnson AP, Morrison D, Speller DC (1995) Current perspectives on glycopeptide resistance. Clin Microbiol Rev 8(4):585–615

    PubMed Central  CAS  PubMed  Google Scholar 

  18. Quintiliani R Jr, Courvalin P (1996) Characterization of Tn1547, a composite transposon flanked by the IS16 and IS256-like elements, that confers vancomycin resistance in Enterococcus faecalis BM4281. Gene 172(1):1–8

    CAS  PubMed  Google Scholar 

  19. Pantosti A, Sanchini A, Monaco M (2007) Mechanisms of antibiotic resistance in Staphylococcus aureus. Futur Microbiol 2(3):323–334. doi:10.2217/17460913.2.3.323

    CAS  Google Scholar 

  20. Argudin MA, Mendoza MC, Rodicio MR (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2(7):1751–1773. doi:10.3390/toxins2071751

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Altboum Z, Hertman I, Sarid S (1985) Penicillinase plasmid-linked genetic determinants for enterotoxins B and C1 production in Staphylococcus aureus. Infect Immun 47(2):514–521

    PubMed Central  CAS  PubMed  Google Scholar 

  22. Jackson MP, Iandolo JJ (1986) Cloning and expression of the exfoliative toxin B gene from Staphylococcus aureus. J Bacteriol 166(2):574–580

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Bukowski M, Wladyka B, Dubin G (2010) Exfoliative toxins of Staphylococcus aureus. Toxins 2(5):1148–1165. doi:10.3390/toxins2051148

    PubMed Central  CAS  PubMed  Google Scholar 

  24. Yamaguchi T, Hayashi T, Takami H, Ohnishi M, Murata T, Nakayama K, Asakawa K, Ohara M, Komatsuzawa H, Sugai M (2001) Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyltransferase, EDIN-C. Infect Immun 69(12):7760–7771. doi:10.1128/IAI.69.12.7760-7771.2001

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Needham C, Noble WC, Dyke KG (1995) The staphylococcal insertion sequence IS257 is active. Plasmid 34(3):198–205. doi:10.1006/plas.1995.0005

    CAS  PubMed  Google Scholar 

  26. Rouch DA, Byrne ME, Kong YC, Skurray RA (1987) The aacA-aphD gentamicin and kanamycin resistance determinant of Tn4001 from Staphylococcus aureus: expression and nucleotide sequence analysis. J Gen Microbiol 133(11):3039–3052

    CAS  PubMed  Google Scholar 

  27. Lyon BR, Gillespie MT, Skurray RA (1987) Detection and characterization of IS256, an insertion sequence in Staphylococcus aureus. J Gen Microbiol 133(11):3031–3038

    CAS  PubMed  Google Scholar 

  28. Lindsay JA (2010) Genomic variation and evolution of Staphylococcus aureus. Int J Med Microbiol 300(2–3):98–103. doi:10.1016/j.ijmm.2009.08.013

    CAS  PubMed  Google Scholar 

  29. Rowland SJ, Dyke KG (1989) Characterization of the staphylococcal beta-lactamase transposon Tn552. EMBO J 8(9):2761–2773

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187(7):2426–2438. doi:10.1128/JB.187.7.2426-2438.2005

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Trees DL, Iandolo JJ (1988) Identification of a Staphylococcus aureus transposon (Tn4291) that carries the methicillin resistance gene(s). J Bacteriol 170(1):149–154

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Guinane CM, Penades JR, Fitzgerald JR (2011) The role of horizontal gene transfer in Staphylococcus aureus host adaptation. Virulence 2(3):241–243

    PubMed  Google Scholar 

  33. Novick RP (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49(2):93–105

    CAS  PubMed  Google Scholar 

  34. Xia G, Wolz C (2013) Phages of Staphylococcus aureus and their impact on host evolution. Infection, genetics and evolution. J Mol Epidemiol Evol Genet Infect Dis. doi:10.1016/j.meegid.2013.04.022

  35. Deghorain M, Van Melderen L (2012) The Staphylococci phages family: an overview. Viruses 4(12):3316–3335

    PubMed Central  PubMed  Google Scholar 

  36. Christie GE, Dokland T (2012) Pirates of the Caudovirales. Virology 434(2):210–221. doi:10.1016/j.virol.2012.10.028

    PubMed Central  CAS  PubMed  Google Scholar 

  37. Rippon JE (1952) A new serological division of Staphylococcus aureus bacteriophages: group G. Nature 170(4320):287

    CAS  PubMed  Google Scholar 

  38. Rippon JE (1956) The classification of bacteriophages lysing staphylococci. J Hyg 54(2):213–226

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Ackermann HW (1975) Classification of the bacteriophages of Gram-positive cocci: Micrococcus, Staphylococcus, and Streptococcus. Pathologie-Biologie 23(3):247–253

    CAS  PubMed  Google Scholar 

  40. Kwan T, Liu J, DuBow M, Gros P, Pelletier J (2005) The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci USA 102(14):5174–5179. doi:10.1073/pnas.0501140102

    PubMed Central  CAS  PubMed  Google Scholar 

  41. Deghorain M, Bobay LM, Smeesters PR, Bousbata S, Vermeersch M, Perez-Morga D, Dreze PA, Rocha EP, Touchon M, Van Melderen L (2012) Characterization of novel phages isolated in coagulase-negative staphylococci reveals evolutionary relationships with Staphylococcus aureus phages. J Bacteriol 194(21):5829–5839. doi:10.1128/JB.01085-12

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Goerke C, Pantucek R, Holtfreter S, Schulte B, Zink M, Grumann D, Broker BM, Doskar J, Wolz C (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191(11):3462–3468. doi:10.1128/JB.01804-08

    PubMed Central  CAS  PubMed  Google Scholar 

  43. McCarthy AJ, van Wamel W, Vandendriessche S, Larsen J, Denis O, Garcia-Graells C, Uhlemann AC, Lowy FD, Skov R, Lindsay JA (2012) Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl Environ Microbiol 78(24):8845–8848. doi:10.1128/AEM.02398-12

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Sumby P, Waldor MK (2003) Transcription of the toxin genes present within the Staphylococcal phage phiSa3ms is intimately linked with the phage’s life cycle. J Bacteriol 185(23):6841–6851

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Wagner PL, Waldor MK (2002) Bacteriophage control of bacterial virulence. Infect Immun 70(8):3985–3993

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Mir-Sanchis I, Martinez-Rubio R, Marti M, Chen J, Lasa I, Novick RP, Tormo-Mas MA, Penades JR (2012) Control of Staphylococcus aureus pathogenicity island excision. Mol Microbiol 85(5):833–845. doi:10.1111/j.1365-2958.2012.08145.x

    CAS  PubMed  Google Scholar 

  47. Ram G, Chen J, Kumar K, Ross HF, Ubeda C, Damle PK, Lane KD, Penades JR, Christie GE, Novick RP (2012) Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc Natl Acad Sci USA 109(40):16300–16305. doi:10.1073/pnas.1204615109

    PubMed Central  CAS  PubMed  Google Scholar 

  48. Dearborn AD, Dokland T (2012) Mobilization of pathogenicity islands by Staphylococcus aureus strain Newman bacteriophages. Bacteriophage 2(2):70–78

    PubMed Central  PubMed  Google Scholar 

  49. Christie GE, Matthews AM, King DG, Lane KD, Olivarez NP, Tallent SM, Gill SR, Novick RP (2010) The complete genomes of Staphylococcus aureus bacteriophages 80 and 80alpha—implications for the specificity of SaPI mobilization. Virology 407(2):381–390. doi:10.1016/j.virol.2010.08.036

    PubMed Central  CAS  PubMed  Google Scholar 

  50. Subedi A, Ubeda C, Adhikari RP, Penades JR, Novick RP (2007) Sequence analysis reveals genetic exchanges and intraspecific spread of SaPI2, a pathogenicity island involved in menstrual toxic shock. Microbiology 153(Pt 10):3235–3245. doi:10.1099/mic.0.2007/006932-0

    CAS  PubMed  Google Scholar 

  51. Novick RP, Subedi A (2007) The SaPIs: mobile pathogenicity islands of Staphylococcus. Chem Immunol Allergy 93:42–57. doi:10.1159/0000100857

    CAS  PubMed  Google Scholar 

  52. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190(1):300–310. doi:10.1128/JB.01000-07

    PubMed Central  CAS  PubMed  Google Scholar 

  53. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367(9512):731–739. doi:10.1016/S0140-6736(06)68231-7

    CAS  PubMed  Google Scholar 

  54. Hacker J, Blum-Oehler G, Muhldorfer I, Tschape H (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23(6):1089–1097

    CAS  PubMed  Google Scholar 

  55. Maiques E, Ubeda C, Tormo MA, Ferrer MD, Lasa I, Novick RP, Penades JR (2007) Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol 189(15):5608–5616. doi:10.1128/JB.00619-07

    PubMed Central  CAS  PubMed  Google Scholar 

  56. Sato’o Y, Omoe K, Ono HK, Nakane A, Hu DL (2013) A novel comprehensive analysis method for Staphylococcus aureus pathogenicity islands. Microbiol Immunol 57(2):91–99. doi:10.1111/1348-0421.12007

    PubMed  Google Scholar 

  57. Viana D, Blanco J, Tormo-Mas MA, Selva L, Guinane CM, Baselga R, Corpa J, Lasa I, Novick RP, Fitzgerald JR, Penades JR (2010) Adaptation of Staphylococcus aureus to ruminant and equine hosts involves SaPI-carried variants of von Willebrand factor-binding protein. Mol Microbiol 77(6):1583–1594

    CAS  PubMed  Google Scholar 

  58. Ubeda C, Barry P, Penades JR, Novick RP (2007) A pathogenicity island replicon in Staphylococcus aureus replicates as an unstable plasmid. Proc Natl Acad Sci USA 104(36):14182–14188. doi:10.1073/pnas.0705994104

    PubMed Central  CAS  PubMed  Google Scholar 

  59. Ubeda C, Tormo MA, Cucarella C, Trotonda P, Foster TJ, Lasa I, Penades JR (2003) Sip, an integrase protein with excision, circularization and integration activities, defines a new family of mobile Staphylococcus aureus pathogenicity islands. Mol Microbiol 49(1):193–210

    CAS  PubMed  Google Scholar 

  60. Ubeda C, Maiques E, Barry P, Matthews A, Tormo MA, Lasa I, Novick RP, Penades JR (2008) SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol Microbiol 67(3):493–503. doi:10.1111/j.1365-2958.2007.06027.x

    CAS  PubMed  Google Scholar 

  61. Ubeda C, Maiques E, Tormo MA, Campoy S, Lasa I, Barbe J, Novick RP, Penades JR (2007) SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol Microbiol 65(1):41–50. doi:10.1111/j.1365-2958.2007.05758.x

    CAS  PubMed  Google Scholar 

  62. Ubeda C, Olivarez NP, Barry P, Wang H, Kong X, Matthews A, Tallent SM, Christie GE, Novick RP (2009) Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol Microbiol 72(1):98–108

    PubMed Central  CAS  PubMed  Google Scholar 

  63. Tormo MA, Ferrer MD, Maiques E, Ubeda C, Selva L, Lasa I, Calvete JJ, Novick RP, Penades JR (2008) Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J Bacteriol 190(7):2434–2440. doi:10.1128/JB.01349-07

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Tormo-Mas MA, Mir I, Shrestha A, Tallent SM, Campoy S, Lasa I, Barbe J, Novick RP, Christie GE, Penades JR (2010) Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465(7299):779–782. doi:10.1038/nature09065

    PubMed Central  CAS  PubMed  Google Scholar 

  65. Schelin J, Wallin-Carlquist N, Cohn MT, Lindqvist R, Barker GC, Radstrom P (2011) The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2(6):580–592. doi:10.4161/viru.2.6.18122

    PubMed Central  PubMed  Google Scholar 

  66. Pinchuk IV, Beswick EJ, Reyes VE (2010) Staphylococcal enterotoxins. Toxins 2(8):2177–2197. doi:10.3390/toxins2082177

    PubMed Central  CAS  PubMed  Google Scholar 

  67. Ortega E, Abriouel H, Lucas R, Galvez A (2010) Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins 2(8):2117–2131. doi:10.3390/toxins2082117

    PubMed Central  PubMed  Google Scholar 

  68. Hennekinne JA, De Buyser ML, Dragacci S (2012) Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36(4):815–836. doi:10.1111/j.1574-6976.2011.00311.x

    CAS  PubMed  Google Scholar 

  69. Wilson GJ, Seo KS, Cartwright RA, Connelley T, Chuang-Smith ON, Merriman JA, Guinane CM, Park JY, Bohach GA, Schlievert PM, Morrison WI, Fitzgerald JR (2011) A novel core genome-encoded superantigen contributes to lethality of community-associated MRSA necrotizing pneumonia. PLoS Pathog 7:e1002271

    PubMed Central  CAS  PubMed  Google Scholar 

  70. Letertre C, Perelle S, Dilasser F, Fach P (2003) Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol 95(1):38–43

    CAS  PubMed  Google Scholar 

  71. Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G (2001) egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166(1):669–677

    CAS  PubMed  Google Scholar 

  72. Monday SR, Bohach GA (2001) Genes encoding staphylococcal enterotoxins G and I are linked and separated by DNA related to other staphylococcal enterotoxins. J Nat Toxins 10(1):1–8

    CAS  PubMed  Google Scholar 

  73. Thomas DY, Jarraud S, Lemercier B, Cozon G, Echasserieau K, Etienne J, Gougeon ML, Lina G, Vandenesch F (2006) Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun 74(8):4724–4734. doi:10.1128/IAI.00132-06

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Thomas D, Chou S, Dauwalder O, Lina G (2007) Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 93:24–41. doi:10.1159/0000100856

    CAS  PubMed  Google Scholar 

  75. Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2(5):376–381. doi:10.1093/embo-reports/kve097

    PubMed Central  CAS  PubMed  Google Scholar 

  76. Ochman H, Lerat E, Daubin V (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci USA 102(Suppl 1):6595–6599. doi:10.1073/pnas.0502035102

    PubMed Central  CAS  PubMed  Google Scholar 

  77. Hentschel U, Hacker J (2001) Pathogenicity islands: the tip of the iceberg. Microbes Infect 3(7):545–548

    CAS  PubMed  Google Scholar 

  78. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2(5):414–424. doi:10.1038/nrmicro884

    CAS  PubMed  Google Scholar 

  79. Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updates 6(1):41–52

    CAS  Google Scholar 

  80. Lina G, Bohach GA, Nair SP, Hiramatsu K, Jouvin-Marche E, Mariuzza R, International Nomenclature Committee for Staphylococcal S (2004) Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis 189(12):2334–2336. doi:10.1086/420852

    PubMed  Google Scholar 

  81. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101(26):9786–9791. doi:10.1073/pnas.0402521101

    PubMed Central  CAS  PubMed  Google Scholar 

  82. Tsuru T, Kobayashi I (2008) Multiple genome comparison within a bacterial species reveals a unit of evolution spanning two adjacent genes in a tandem paralog cluster. Mol Biol Evol 25(11):2457–2473. doi:10.1093/molbev/msn192

    PubMed Central  CAS  PubMed  Google Scholar 

  83. Schmidt H, Hensel M (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17(1):14–56

    PubMed Central  CAS  PubMed  Google Scholar 

  84. Waldron DE, Lindsay JA (2006) Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188(15):5578–5585. doi:10.1128/JB.00418-06

    PubMed Central  CAS  PubMed  Google Scholar 

  85. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM, Ferguson DJ, Hood DW (2007) Novel type IV secretion system involved in propagation of genomic islands. J Bacteriol 189(3):761–771. doi:10.1128/JB.01327-06

    PubMed Central  CAS  PubMed  Google Scholar 

  86. Hooper SD, Berg OG (2002) Detection of genes with atypical nucleotide sequence in microbial genomes. J Mol Evol 54(3):365–375. doi:10.1007/s00239-001-0051-8

    CAS  PubMed  Google Scholar 

  87. Karlin S (2001) Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol 9(7):335–343

    CAS  PubMed  Google Scholar 

  88. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95(16):9413–9417

    PubMed Central  CAS  PubMed  Google Scholar 

  89. Severin A, Wu SW, Tabei K, Tomasz A (2005) High-level (beta)-lactam resistance and cell wall synthesis catalyzed by the mecA homologue of Staphylococcus sciuri introduced into Staphylococcus aureus. J Bacteriol 187(19):6651–6658. doi:10.1128/JB.187.19.6651-6658.2005

    PubMed Central  CAS  PubMed  Google Scholar 

  90. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, Jamklang M, Chavalit T, Song JH, Hiramatsu K (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(3):1001–1012. doi:10.1128/AAC.50.3.1001-1012.2006

    PubMed Central  CAS  PubMed  Google Scholar 

  91. de Lencastre H, Oliveira D, Tomasz A (2007) Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr Opin Microbiol 10(5):428–435. doi:10.1016/j.mib.2007.08.003

    PubMed Central  PubMed  Google Scholar 

  92. International Working Group on the Classification of Staphylococcal Cassette Chromosome E (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53(12):4961–4967. doi:10.1128/AAC.00579-09

    Google Scholar 

  93. Luong TT, Ouyang S, Bush K, Lee CY (2002) Type 1 capsule genes of Staphylococcus aureus are carried in a staphylococcal cassette chromosome genetic element. J Bacteriol 184(13):3623–3629

    PubMed Central  CAS  PubMed  Google Scholar 

  94. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359(9320):1819–1827

    CAS  PubMed  Google Scholar 

  95. Fraser JD, Proft T (2008) The bacterial superantigen and superantigen-like proteins. Immunol Rev 225:226–243. doi:10.1111/j.1600-065X.2008.00681.x

    CAS  PubMed  Google Scholar 

  96. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, Leitch CD, Daum RS (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279(8):593–598

    CAS  PubMed  Google Scholar 

  97. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, Warner M, Livermore DM, Cookson BD, Participants UE (2001) Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48(1):143–144

    CAS  PubMed  Google Scholar 

  98. Dufour P, Gillet Y, Bes M, Lina G, Vandenesch F, Floret D, Etienne J, Richet H (2002) Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Infect Dis 35(7):819–824. doi:10.1086/342576

    CAS  PubMed  Google Scholar 

  99. Chiang YC, Liao WW, Fan CM, Pai WY, Chiou CS, Tsen HY (2008) PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 121(1):66–73. doi:10.1016/j.ijfoodmicro.2007.10.005

    CAS  PubMed  Google Scholar 

  100. Makris G, Wright JD, Ingham E, Holland KT (2004) The hyaluronate lyase of Staphylococcus aureus—a virulence factor? Microbiology 150(Pt 6):2005–2013. doi:10.1099/mic.0.26942-0

    CAS  PubMed  Google Scholar 

  101. Barrio MB, Rainard P, Prevost G (2006) LukM/LukF’-PV is the most active Staphylococcus aureus leukotoxin on bovine neutrophils. Microbes Infect 8(8):2068–2074. doi:10.1016/j.micinf.2006.03.004

    CAS  PubMed  Google Scholar 

  102. Stec-Niemczyk J, Pustelny K, Kisielewska M, Bista M, Boulware KT, Stennicke HR, Thogersen IB, Daugherty PS, Enghild JJ, Baczynski K, Popowicz GM, Dubin A, Potempa J, Dubin G (2009) Structural and functional characterization of SplA, an exclusively specific protease of Staphylococcus aureus. Biochem J 419(3):555–564. doi:10.1042/BJ20081351

    CAS  PubMed  Google Scholar 

  103. Yamaguchi T, Nishifuji K, Sasaki M, Fudaba Y, Aepfelbacher M, Takata T, Ohara M, Komatsuzawa H, Amagai M, Sugai M (2002) Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect Immun 70(10):5835–5845

    PubMed Central  CAS  PubMed  Google Scholar 

  104. Highlander SK, Hulten KG, Qin X, Jiang H, Yerrapragada S, Mason EO Jr, Shang Y, Williams TM, Fortunov RM, Liu Y, Igboeli O, Petrosino J, Tirumalai M, Uzman A, Fox GE, Cardenas AM, Muzny DM, Hemphill L, Ding Y, Dugan S, Blyth PR, Buhay CJ, Dinh HH, Hawes AC, Holder M, Kovar CL, Lee SL, Liu W, Nazareth LV, Wang Q, Zhou J, Kaplan SL, Weinstock GM (2007) Subtlegenetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol 7:99. doi:10.1186/1471-2180-7-99

    PubMed Central  PubMed  Google Scholar 

  105. Mehlin C, Headley CM, Klebanoff SJ (1999) An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J Exp Med 189(6):907–918

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Vuong C, Durr M, Carmody AB, Peschel A, Klebanoff SJ, Otto M (2004) Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epidermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modulins. Cell Microbiol 6(8):753–759. doi:10.1111/j.1462-5822.2004.00401.x

    CAS  PubMed  Google Scholar 

  107. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45(5):1323–1336. doi:10.1128/AAC.45.5.1323-1336.2001

    PubMed Central  CAS  PubMed  Google Scholar 

  108. Ito T, Katayama Y, Hiramatsu K (1999) Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 43(6):1449–1458

    PubMed Central  CAS  PubMed  Google Scholar 

  109. Ma XX, Ito T, Tiensasitorn C, Jamklang M, Chongtrakool P, Boyle-Vavra S, Daum RS, Hiramatsu K (2002) Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 46(4):1147–1152

    PubMed Central  CAS  PubMed  Google Scholar 

  110. Ma XX, Ito T, Chongtrakool P, Hiramatsu K (2006) Predominance of clones carrying Panton-Valentine leukocidin genes among methicillin-resistant Staphylococcus aureus strains isolated in Japanese hospitals from 1979 to 1985. J Clin Microbiol 44(12):4515–4527. doi:10.1128/JCM.00985-06

    PubMed Central  CAS  PubMed  Google Scholar 

  111. Milheirico C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: ‘SCCmec IV multiplex’. J Antimicrob Chemother 60(1):42–48. doi:10.1093/jac/dkm112

    CAS  PubMed  Google Scholar 

  112. Berglund C, Ito T, Ma XX, Ikeda M, Watanabe S, Soderquist B, Hiramatsu K (2009) Genetic diversity of methicillin-resistant Staphylococcus aureus carrying type IV SCCmec in Orebro County and the western region of Sweden. J Antimicrob Chemother 63(1):32–41. doi:10.1093/jac/dkn435

    CAS  PubMed  Google Scholar 

  113. Kwon NH, Park KT, Moon JS, Jung WK, Kim SH, Kim JM, Hong SK, Koo HC, Joo YS, Park YH (2005) Staphylococcal cassette chromosome mec (SCCmec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J Antimicrob Chemother 56(4):624–632. doi:10.1093/jac/dki306

    CAS  PubMed  Google Scholar 

  114. Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48(7):2637–2651. doi:10.1128/AAC.48.7.2637-2651.2004

    PubMed Central  CAS  PubMed  Google Scholar 

  115. Berglund C, Ito T, Ikeda M, Ma XX, Soderquist B, Hiramatsu K (2008) Novel type of staphylococcal cassette chromosome mec in a methicillin-resistant Staphylococcus aureus strain isolated in Sweden. Antimicrob Agents Chemother 52(10):3512–3516. doi:10.1128/AAC.00087-08

    PubMed Central  CAS  PubMed  Google Scholar 

  116. Zhang K, McClure JA, Elsayed S, Conly JM (2009) Novel staphylococcal cassette chromosome mec type, tentatively designated type VIII, harboring class A mec and type 4 ccr gene complexes in a Canadian epidemic strain of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 53(2):531–540. doi:10.1128/AAC.01118-08

    PubMed Central  CAS  PubMed  Google Scholar 

  117. Li S, Skov RL, Han X, Larsen AR, Larsen J, Sorum M, Wulf M, Voss A, Hiramatsu K, Ito T (2011) Novel types of staphylococcal cassette chromosome mec elements identified in clonal complex 398 methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 55(6):3046–3050. doi:10.1128/AAC.01475-10

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial Support from Specific University Research (MSMT No. 20/2013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lamine Baba-Moussa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alibayov, B., Baba-Moussa, L., Sina, H. et al. Staphylococcus aureus mobile genetic elements. Mol Biol Rep 41, 5005–5018 (2014). https://doi.org/10.1007/s11033-014-3367-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3367-3

Keywords

Navigation