1887

Abstract

Staphylococci are Gram-positive spherical bacteria of enormous clinical and biotechnological relevance. has been extensively studied as a model pathogen. A plethora of methods and molecular tools has been developed for genetic modification of at least ten different staphylococcal species to date. Here we review recent developments of various genetic tools and molecular methods for staphylococcal research, which include reporter systems and vectors for controllable gene expression, gene inactivation, gene essentiality testing, chromosomal integration and transposon delivery. It is furthermore illustrated how mutant strain construction by homologous or site-specific recombination benefits from sophisticated counterselection methods. The underlying genetic components have been shown to operate in wild-type staphylococci or modified chassis strains. Finally, possible future developments in the field of applied genetics are highlighted.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.061705-0
2013-03-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/3/421.html?itemId=/content/journal/micro/10.1099/mic.0.061705-0&mimeType=html&fmt=ahah

References

  1. Andersen J. B., Sternberg C., Poulsen L. K., Bjørn S. P., Givskov M., Molin S. ( 1998). New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64:2240–2246[PubMed]
    [Google Scholar]
  2. Arnaud M., Chastanet A., Débarbouillé M. ( 2004). New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70:6887–6891 [View Article][PubMed]
    [Google Scholar]
  3. Augustin J., Götz F. ( 1990). Transformation of Staphylococcus epidermidis and other staphylococcal species with plasmid DNA by electroporation. FEMS Microbiol Lett 54:203–207 [View Article][PubMed]
    [Google Scholar]
  4. Bae T., Schneewind O. ( 2006). Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58–63 [View Article][PubMed]
    [Google Scholar]
  5. Bae T., Banger A. K., Wallace A., Glass E. M., Aslund F., Schneewind O., Missiakas D. M. ( 2004). Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci U S A 101:12312–12317 [View Article][PubMed]
    [Google Scholar]
  6. Bae T., Glass E. M., Schneewind O., Missiakas D. ( 2008). Generating a collection of insertion mutations in the Staphylococcus aureus genome using bursa aurealis . Methods Mol Biol 416:103–116 [View Article][PubMed]
    [Google Scholar]
  7. Bateman B. T., Donegan N. P., Jarry T. M., Palma M., Cheung A. L. ( 2001). Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect Immun 69:7851–7857 [View Article][PubMed]
    [Google Scholar]
  8. Benton B. M., Zhang J. P., Bond S., Pope C., Christian T., Lee L., Winterberg K. M., Schmid M. B., Buysse J. M. ( 2004). Large-scale identification of genes required for full virulence of Staphylococcus aureus . J Bacteriol 186:8478–8489[PubMed] [CrossRef]
    [Google Scholar]
  9. Bertram R., Hillen W. ( 2008). The application of Tet repressor in prokaryotic gene regulation and expression. Microb Biotechnol 1:2–16[PubMed]
    [Google Scholar]
  10. Bertram R., Köstner M., Müller J., Vazquez Ramos J., Hillen W. ( 2005). Integrative elements for Bacillus subtilis yielding tetracycline-dependent growth phenotypes. Nucleic Acids Res 33:e153 [View Article][PubMed]
    [Google Scholar]
  11. Bertram R. ( 2010). Tetracycline-dependent gene regulation architectures in bacteria. http://tinyurl.com/tetreg . [PubMed]
    [Google Scholar]
  12. Blake K. L., O'Neill A. J. ( 2013). Transposon library screening for identification of genetic loci participating in intrinsic susceptibility and acquired resistance to antistaphylococcal agents. J Antimicrob Chemother 68:12–16[PubMed] [CrossRef]
    [Google Scholar]
  13. Bose J. L., Fey P. D., Bayles K. W. ( 2013). Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus . Appl Environ Microbiol
    [Google Scholar]
  14. Bramucci M. G., Nagarajan V. ( 1996). Direct selection of cloned DNA in Bacillus subtilis based on sucrose-induced lethality. Appl Environ Microbiol 62:3948–3953[PubMed]
    [Google Scholar]
  15. Brückner R. ( 1992). A series of shuttle vectors for Bacillus subtilis and Escherichia coli . Gene 122:187–192 [View Article][PubMed]
    [Google Scholar]
  16. Brückner R. ( 1997). Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus . FEMS Microbiol Lett 151:1–8 [View Article][PubMed]
    [Google Scholar]
  17. Brückner R., Zyprian E., Matzura H. ( 1984). Expression of a chloramphenicol-resistance determinant carried on hybrid plasmids in gram-positive and gram-negative bacteria. Gene 32:151–160 [View Article][PubMed]
    [Google Scholar]
  18. Charpentier E., Anton A. I., Barry P., Alfonso B., Fang Y., Novick R. P. ( 2004). Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 70:6076–6085 [View Article][PubMed]
    [Google Scholar]
  19. Chaudhuri R. R., Allen A. G., Owen P. J., Shalom G., Stone K., Harrison M., Burgis T. A., Lockyer M., Garcia-Lara J. & other authors ( 2009). Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). BMC Genomics 10:291 [View Article][PubMed]
    [Google Scholar]
  20. Cheetham G. M., Steitz T. A. ( 2000). Insights into transcription: structure and function of single-subunit DNA-dependent RNA polymerases. Curr Opin Struct Biol 10:117–123 [View Article][PubMed]
    [Google Scholar]
  21. Cheung A. L., Nast C. C., Bayer A. S. ( 1998). Selective activation of sar promoters with the use of green fluorescent protein transcriptional fusions as the detection system in the rabbit endocarditis model. Infect Immun 66:5988–5993[PubMed]
    [Google Scholar]
  22. Corbiere Morot-Bizot S., Leroy S., Talon R. ( 2007). Monitoring of staphylococcal starters in two French processing plants manufacturing dry fermented sausages. J Appl Microbiol 102:238–244 [View Article][PubMed]
    [Google Scholar]
  23. Corbisier P., Ji G., Nuyts G., Mergeay M., Silver S. ( 1993). luxAB gene fusions with the arsenic and cadmium resistance operons of Staphylococcus aureus plasmid pI258. FEMS Microbiol Lett 110:231–238 [View Article][PubMed]
    [Google Scholar]
  24. Corrigan R. M., Foster T. J. ( 2009). An improved tetracycline-inducible expression vector for Staphylococcus aureus . Plasmid 61:126–129 [View Article][PubMed]
    [Google Scholar]
  25. D’Elia M. A., Pereira M. P., Chung Y. S., Zhao W., Chau A., Kenney T. J., Sulavik M. C., Black T. A., Brown E. D. ( 2006). Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 188:4183–4189 [View Article][PubMed]
    [Google Scholar]
  26. Datsenko K. A., Wanner B. L. ( 2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  27. DeLeo F. R., Otto M., Kreiswirth B. N., Chambers H. F. ( 2010). Community-associated meticillin-resistant Staphylococcus aureus . Lancet 375:1557–1568 [View Article][PubMed]
    [Google Scholar]
  28. Fan F., Lunsford R. D., Sylvester D., Fan J., Celesnik H., Iordanescu S., Rosenberg M., McDevitt D. ( 2001). Regulated ectopic expression and allelic-replacement mutagenesis as a method for gene essentiality testing in Staphylococcus aureus . Plasmid 46:71–75 [View Article][PubMed]
    [Google Scholar]
  29. Felden B., Vandenesch F., Bouloc P., Romby P. ( 2011). The Staphylococcus aureus RNome and its commitment to virulence. PLoS Pathog 7:e1002006 [View Article][PubMed]
    [Google Scholar]
  30. Fey P. D., Endres J. L., Yajjala V. K., Widhelm T. J., Boissy R. J., Bose J. L., Bayles K. W. ( 2013). A genetic resource for rapid and comprehensive phenotype screening of non-essential Staphylococcus aureus genes . mBio[PubMed]
    [Google Scholar]
  31. Firth N., Apisiridej S., Berg T., O’Rourke B. A., Curnock S., Dyke K. G., Skurray R. A. ( 2000). Replication of staphylococcal multiresistance plasmids. J Bacteriol 182:2170–2178 [View Article][PubMed]
    [Google Scholar]
  32. Forsyth R. A., Haselbeck R. J., Ohlsen K. L., Yamamoto R. T., Xu H., Trawick J. D., Wall D., Wang L., Brown-Driver V. & other authors ( 2002). A genome-wide strategy for the identification of essential genes in Staphylococcus aureus . Mol Microbiol 43:1387–1400 [View Article][PubMed]
    [Google Scholar]
  33. Francis K. P., Joh D., Bellinger-Kawahara C., Hawkinson M. J., Purchio T. F., Contag P. R. ( 2000). Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect Immun 68:3594–3600 [View Article][PubMed]
    [Google Scholar]
  34. Franke G. C., Dobinsky S., Mack D., Wang C. J., Sobottka I., Christner M., Knobloch J. K., Horstkotte M. A., Aepfelbacher M., Rohde H. ( 2007). Expression and functional characterization of gfpmut3.1 and its unstable variants in Staphylococcus epidermidis . J Microbiol Methods 71:123–132 [View Article][PubMed]
    [Google Scholar]
  35. Gauger T., Weihs F., Mayer S., Krismer B., Liese J., Kull M., Bertram R. ( 2012). Intracellular monitoring of target protein production in Staphylococcus aureus by peptide tag-induced reporter fluorescence. Microb Biotechnol 5:129–134 [View Article][PubMed]
    [Google Scholar]
  36. Geiger T., Francois P., Liebeke M., Fraunholz M., Goerke C., Krismer B., Schrenzel J., Lalk M., Wolz C. ( 2012). The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog 8:e1003016 [View Article][PubMed]
    [Google Scholar]
  37. Geissendörfer M., Hillen W. ( 1990). Regulated expression of heterologous genes in Bacillus subtilis using the Tn10 encoded tet regulatory elements. Appl Microbiol Biotechnol 33:657–663 [View Article][PubMed]
    [Google Scholar]
  38. Gennaro M. L., Kornblum J., Novick R. P. ( 1987). A site-specific recombination function in Staphylococcus aureus plasmids. J Bacteriol 169:2601–2610[PubMed]
    [Google Scholar]
  39. Ghebremedhin B., Layer F., König W., König B. ( 2008). Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol 46:1019–1025 [View Article][PubMed]
    [Google Scholar]
  40. Goryshin I. Y., Jendrisak J., Hoffman L. M., Meis R., Reznikoff W. S. ( 2000). Insertional transposon mutagenesis by electroporation of released Tn5 transposition complexes. Nat Biotechnol 18:97–100 [View Article][PubMed]
    [Google Scholar]
  41. Götz F. ( 1990). Staphylococcus carnosus: a new host organism for gene cloning and protein production. Soc Appl Bacteriol Symp Ser 69:s1949S–53S [View Article][PubMed]
    [Google Scholar]
  42. Götz F., Schumacher B. ( 1987). Improvements of protoplast transformation in Staphylococcus carnosus . FEMS Microbiol Lett 40:285–288 [View Article]
    [Google Scholar]
  43. Götz F., Bannerman T., Schleifer K.-H. ( 2006). The genera Staphylococcus and Macrococcus . Prokaryotes5–75 Dworkin M. New York: Springer; [View Article]
    [Google Scholar]
  44. Grindley N. D., Whiteson K. L., Rice P. A. ( 2006). Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605 [View Article][PubMed]
    [Google Scholar]
  45. Grkovic S., Brown M. H., Skurray R. A. ( 2002). Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66:671–701 [View Article][PubMed]
    [Google Scholar]
  46. Grkovic S., Brown M. H., Hardie K. M., Firth N., Skurray R. A. ( 2003). Stable low-copy-number Staphylococcus aureus shuttle vectors. Microbiology 149:785–794 [View Article][PubMed]
    [Google Scholar]
  47. Grueter L., Koenig O., Laufs R. ( 1991). Transposon mutagenesis in Staphylococcus epidermidis using the Enterococcus faecalis transposon Tn917 . FEMS Microbiol Lett 82:215–218 [View Article][PubMed]
    [Google Scholar]
  48. Gründling A., Schneewind O. ( 2007a). Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus . Proc Natl Acad Sci U S A 104:8478–8483 [View Article][PubMed]
    [Google Scholar]
  49. Gründling A., Schneewind O. ( 2007b). Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus . J Bacteriol 189:2521–2530 [View Article][PubMed]
    [Google Scholar]
  50. Halfmann G., Götz F., Lubitz W. ( 1993). Expression of bacteriophage PhiX174 lysis gene E in Staphylococcus carnosus TM300. FEMS Microbiol Lett 108:139–143 [View Article][PubMed]
    [Google Scholar]
  51. Hayes F. ( 2003). Transposon-based strategies for microbial functional genomics and proteomics. Annu Rev Genet 37:3–29 [View Article][PubMed]
    [Google Scholar]
  52. Helle L., Kull M., Mayer S., Marincola G., Zelder M. E., Goerke C., Wolz C., Bertram R. ( 2011). Vectors for improved Tet repressor-dependent gradual gene induction or silencing in Staphylococcus aureus . Microbiology 157:3314–3323 [View Article][PubMed]
    [Google Scholar]
  53. Hentschel E., Will C., Mustafi N., Burkovski A., Rehm N., Frunzke J. ( 2012). Destabilized eYFP variants for dynamic gene expression studies in Corynebacterium glutamicum . Microb Biotechnol [View Article][PubMed]
    [Google Scholar]
  54. Herbert S., Ziebandt A. K., Ohlsen K., Schäfer T., Hecker M., Albrecht D., Novick R., Götz F. ( 2010). Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 78:2877–2889 [View Article][PubMed]
    [Google Scholar]
  55. Huber J., Donald R. G., Lee S. H., Jarantow L. W., Salvatore M. J., Meng X., Painter R., Onishi R. H., Occi J., Dorso K. ( 2009). Chemical genetic identification of peptidoglycan inhibitors potentiating carbapenem activity against methicillin-resistant Staphylococcus aureus . Chem Biol 16:837–848 [View Article][PubMed]
    [Google Scholar]
  56. Hueck C. J., Hillen W., Saier M. H. Jr ( 1994). Analysis of a cis-active sequence mediating catabolite repression in gram-positive bacteria. Res Microbiol 145:503–518 [View Article][PubMed]
    [Google Scholar]
  57. Hussain M., Becker K., von Eiff C., Schrenzel J., Peters G., Herrmann M. ( 2001). Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J Bacteriol 183:6778–6786 [View Article][PubMed]
    [Google Scholar]
  58. Jana M., Luong T. T., Komatsuzawa H., Shigeta M., Lee C. Y. ( 2000). A method for demonstrating gene essentiality in Staphylococcus aureus . Plasmid 44:100–104 [View Article][PubMed]
    [Google Scholar]
  59. Ji Y., Marra A., Rosenberg M., Woodnutt G. ( 1999). Regulated antisense RNA eliminates alpha-toxin virulence in Staphylococcus aureus infection. J Bacteriol 181:6585–6590[PubMed]
    [Google Scholar]
  60. Ji Y., Zhang B., Van S. F., Horn, Warren P., Woodnutt G., Burnham M. K., Rosenberg M. ( 2001). Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA. Science 293:2266–2269 [View Article][PubMed]
    [Google Scholar]
  61. Kahl B. C., Goulian M., van Wamel W., Herrmann M., Simon S. M., Kaplan G., Peters G., Cheung A. L. ( 2000). Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect Immun 68:5385–5392 [View Article][PubMed]
    [Google Scholar]
  62. Kamionka A., Bogdanska-Urbaniak J., Scholz O., Hillen W. ( 2004). Two mutations in the tetracycline repressor change the inducer anhydrotetracycline to a corepressor. Nucleic Acids Res 32:842–847 [View Article][PubMed]
    [Google Scholar]
  63. Kato F., Sugai M. ( 2011). A simple method of markerless gene deletion in Staphylococcus aureus . J Microbiol Methods 87:76–81 [View Article][PubMed]
    [Google Scholar]
  64. Kellner R., Jung G., Hörner T., Zähner H., Schnell N., Entian K. D., Götz F. ( 1988). Gallidermin: a new lanthionine-containing polypeptide antibiotic. Eur J Biochem 177:53–59 [View Article][PubMed]
    [Google Scholar]
  65. Kloos W., Schleifer K. H., Götz F. ( 1991). The genus Staphylococcus . The Prokaryotes1369–1420 Balows B., Trüper H. G., Dworkin M., Harder W., Schleifer K. H. London: Springer;
    [Google Scholar]
  66. Klotzsche M., Berens C., Hillen W. ( 2005). A peptide triggers allostery in tet repressor by binding to a unique site. J Biol Chem 280:24591–24599 [View Article][PubMed]
    [Google Scholar]
  67. Kreiswirth B. N., Löfdahl S., Betley M. J., O’Reilly M., Schlievert P. M., Bergdoll M. S., Novick R. P. ( 1983). The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709–712 [View Article][PubMed]
    [Google Scholar]
  68. Krismer B. ( 1999).galRKETStaphylococcus carnosus
  69. Krismer B., Nega M., Thumm G., Götz F., Peschel A. ( 2012). Highly efficient Staphylococcus carnosus mutant selection system based on suicidal bacteriocin activation. Appl Environ Microbiol 78:1148–1156 [View Article][PubMed]
    [Google Scholar]
  70. Lampe D. J., Churchill M. E., Robertson H. M. ( 1996). A purified mariner transposase is sufficient to mediate transposition in vitro . EMBO J 15:5470–5479[PubMed]
    [Google Scholar]
  71. Lauderdale K. J., Boles B. R., Cheung A. L., Horswill A. R. ( 2009). Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77:1623–1635 [View Article][PubMed]
    [Google Scholar]
  72. Lee C. Y., Iandolo J. J. ( 1986a). Integration of staphylococcal phage L54a occurs by site-specific recombination: structural analysis of the attachment sites. Proc Natl Acad Sci U S A 83:5474–5478 [View Article][PubMed]
    [Google Scholar]
  73. Lee C. Y., Iandolo J. J. ( 1986b). Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J Bacteriol 166:385–391[PubMed]
    [Google Scholar]
  74. Lee C. Y., Buranen S. L., Ye Z. H. ( 1991). Construction of single-copy integration vectors for Staphylococcus aureus . Gene 103:101–105 [View Article][PubMed]
    [Google Scholar]
  75. Lei M. G., Cue D., Alba J., Junecko J., Graham J. W., Lee C. Y. ( 2012). A single copy integration vector that integrates at an engineered site on the Staphylococcus aureus chromosome. BMC Res Notes 5:5 [View Article][PubMed]
    [Google Scholar]
  76. Leibig M., Krismer B., Kolb M., Friede A., Götz F., Bertram R. ( 2008). Marker removal in staphylococci via Cre recombinase and different lox sites. Appl Environ Microbiol 74:1316–1323 [View Article][PubMed]
    [Google Scholar]
  77. Levy S. B., Marshall B. ( 2004). Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:Suppl.S122–S129 [View Article][PubMed]
    [Google Scholar]
  78. Li M., Rigby K., Lai Y., Nair V., Peschel A., Schittek B., Otto M. ( 2009). Staphylococcus aureus mutant screen reveals interaction of the human antimicrobial peptide dermcidin with membrane phospholipids. Antimicrob Agents Chemother 53:4200–4210 [View Article][PubMed]
    [Google Scholar]
  79. Liese J., Rooijakkers S. H., van Strijp J. A., Novick R. P., Dustin M. L. ( 2012). Intravital two-photon microscopy of host-pathogen interactions in a mouse model of Staphylococcus aureus skin abscess formation. Cell Microbiol [View Article][PubMed]
    [Google Scholar]
  80. Liew A. T., Theis T., Jensen S. O., Garcia-Lara J., Foster S. J., Firth N., Lewis P. J., Harry E. J. ( 2011). A simple plasmid-based system that allows rapid generation of tightly controlled gene expression in Staphylococcus aureus . Microbiology 157:666–676 [View Article][PubMed]
    [Google Scholar]
  81. Löfblom J., Kronqvist N., Uhlén M., Ståhl S., Wernérus H. ( 2007). Optimization of electroporation-mediated transformation: Staphylococcus carnosus as model organism. J Appl Microbiol 102:736–747 [View Article][PubMed]
    [Google Scholar]
  82. Lowe A. M., Beattie D. T., Deresiewicz R. L. ( 1998). Identification of novel staphylococcal virulence genes by in vivo expression technology. Mol Microbiol 27:967–976 [View Article][PubMed]
    [Google Scholar]
  83. Lowy F. D. ( 1998). Staphylococcus aureus infections. N Engl J Med 339:520–532 [View Article][PubMed]
    [Google Scholar]
  84. Luong T. T., Lee C. Y. ( 2007). Improved single-copy integration vectors for Staphylococcus aureus . J Microbiol Methods 70:186–190 [View Article][PubMed]
    [Google Scholar]
  85. Mainiero M., Goerke C., Geiger T., Gonser C., Herbert S., Wolz C. ( 2010). Differential target gene activation by the Staphylococcus aureus two-component system saeRS . J Bacteriol 192:613–623 [View Article][PubMed]
    [Google Scholar]
  86. Malone C. L., Boles B. R., Lauderdale K. J., Thoendel M., Kavanaugh J. S., Horswill A. R. ( 2009). Fluorescent reporters for Staphylococcus aureus . J Microbiol Methods 77:251–260 [View Article][PubMed]
    [Google Scholar]
  87. Marlinghaus L., Becker K., Korte M., Neumann S., Gatermann S. G., Szabados F. ( 2012). Construction and characterization of three knockout mutants of the fbl gene in Staphylococcus lugdunensis . APMIS 120:108–116 [View Article][PubMed]
    [Google Scholar]
  88. McNamara P. ( 2008). Genetic manipulation of Staphylococcus aureus . Staphylococcus Molecular Genetics89–130 Lindsay J. A. Norfolk, UK: Caister Academic Press;
    [Google Scholar]
  89. Mei J. M., Nourbakhsh F., Ford C. W., Holden D. W. ( 1997). Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol Microbiol 26:399–407 [View Article][PubMed]
    [Google Scholar]
  90. Meighen E. A. ( 1991). Molecular biology of bacterial bioluminescence. Microbiol Rev 55:123–142[PubMed]
    [Google Scholar]
  91. Meighen E. A. ( 1993). Bacterial bioluminescence: organization, regulation, and application of the lux genes. FASEB J 7:1016–1022[PubMed]
    [Google Scholar]
  92. Mesak L. R., Yim G., Davies J. ( 2009). Improved lux reporters for use in Staphylococcus aureus . Plasmid 61:182–187 [View Article][PubMed]
    [Google Scholar]
  93. Mesak L. R., Qi S., Villanueva I., Miao V., Davies J. ( 2010). Staphylococcus aureus promoter-lux reporters for drug discovery. J Antibiot (Tokyo) 63:492–498 [View Article][PubMed]
    [Google Scholar]
  94. Monk I. R., Foster T. J. ( 2012). Genetic manipulation of Staphylococci-breaking through the barrier. Front Cell Infect Microbiol 2:49[PubMed] [CrossRef]
    [Google Scholar]
  95. Monk I. R., Shah I. M., Xu M., Tan M. W., Foster T. J. ( 2012). Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. MBio 3:e00277-11 [View Article][PubMed]
    [Google Scholar]
  96. Morikawa K., Inose Y., Okamura H., Maruyama A., Hayashi H., Takeyasu K., Ohta T. ( 2003). A new staphylococcal sigma factor in the conserved gene cassette: functional significance and implication for the evolutionary processes. Genes Cells 8:699–712 [View Article][PubMed]
    [Google Scholar]
  97. Morikawa K., Takemura A. J., Inose Y., Tsai M., Nguyen Thi T., Ohta T., Msadek T. ( 2012). Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus . PLoS Pathog 8:e1003003 [View Article][PubMed]
    [Google Scholar]
  98. Murray R. W., Melchior E. P., Hagadorn J. C., Marotti K. R. ( 2001). Staphylococcus aureus cell extract transcription-translation assay: firefly luciferase reporter system for evaluating protein translation inhibitors. Antimicrob Agents Chemother 45:1900–1904 [View Article][PubMed]
    [Google Scholar]
  99. Novick R. P. ( 1989). Staphylococcal plasmids and their replication. Annu Rev Microbiol 43:537–563 [View Article][PubMed]
    [Google Scholar]
  100. Novick R. P. ( 1991). Genetic systems in staphylococci. Methods Enzymol 204:587–636 [View Article][PubMed]
    [Google Scholar]
  101. O’Reilly M., de Azavedo J. C., Kennedy S., Foster T. J. ( 1986). Inactivation of the alpha-haemolysin gene of Staphylococcus aureus 8325-4 by site-directed mutagenesis and studies on the expression of its haemolysins. Microb Pathog 1:125–138 [View Article][PubMed]
    [Google Scholar]
  102. Ohlsen K., Koller K. P., Hacker J. ( 1997). Analysis of expression of the alpha-toxin gene (hla) of Staphylococcus aureus by using a chromosomally encoded hla:lacZ gene fusion. Infect Immun 65:3606–3614[PubMed]
    [Google Scholar]
  103. Otto M. ( 2009). Staphylococcus epidermidis–the ‘accidental’ pathogen. Nat Rev Microbiol 7:555–567 [View Article][PubMed]
    [Google Scholar]
  104. Otto M., Süßmuth R., Jung G., Götz F. ( 1998). Structure of the pheromone peptide of the Staphylococcus epidermidis agr system. FEBS Lett 424:89–94 [View Article][PubMed]
    [Google Scholar]
  105. Pagels M., Fuchs S., Pané-Farré J., Kohler C., Menschner L., Hecker M., McNamarra P. J., Bauer M. C., von Wachenfeldt C. & other authors ( 2010). Redox sensing by a Rex-family repressor is involved in the regulation of anaerobic gene expression in Staphylococcus aureus . Mol Microbiol 76:1142–1161 [View Article][PubMed]
    [Google Scholar]
  106. Pajunen M. I., Pulliainen A. T., Finne J., Savilahti H. ( 2005). Generation of transposon insertion mutant libraries for Gram-positive bacteria by electroporation of phage Mu DNA transposition complexes. Microbiology 151:1209–1218 [View Article][PubMed]
    [Google Scholar]
  107. Pantůček R., Svec P., Dajcs J. J., Machová I., Cernohlávková J., Sedo O., Gelbíčová T., Mašlaňová I., Doškař J., Zdráhal Z., Růžičková V., Sedláček I. ( 2013). Staphylococcus petrasii sp. nov. including S. petrasii subsp. petrasii subsp. nov. and S. petrasii subsp. croceilyticus subsp. nov., isolated from human clinical specimens and human ear infections. Syst Appl Microbiol[PubMed]
    [Google Scholar]
  108. Paprotka K., Giese B., Fraunholz M. J. ( 2010). Codon-improved fluorescent proteins in investigation of Staphylococcus aureus host pathogen interactions. J Microbiol Methods 83:82–86 [View Article][PubMed]
    [Google Scholar]
  109. Pédelacq J. D., Cabantous S., Tran T., Terwilliger T. C., Waldo G. S. ( 2006). Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24:79–88 [View Article][PubMed]
    [Google Scholar]
  110. Pereira P. M., Veiga H., Jorge A. M., Pinho M. G. ( 2010). Fluorescent reporters for studies of cellular localization of proteins in Staphylococcus aureus . Appl Environ Microbiol 76:4346–4353 [View Article][PubMed]
    [Google Scholar]
  111. Peschel A., Ottenwälder B., Götz F. ( 1996). Inducible production and cellular location of the epidermin biosynthetic enzyme EpiB using an improved staphylococcal expression system. FEMS Microbiol Lett 137:279–284 [View Article][PubMed]
    [Google Scholar]
  112. Place R. B., Hiestand D., Gallmann H. R., Teuber M. ( 2003). Staphylococcus equorum subsp. linens, subsp. nov., a starter culture component for surface ripened semi-hard cheeses. Syst Appl Microbiol 26:30–37 [View Article][PubMed]
    [Google Scholar]
  113. Pósfai G., Kolisnychenko V., Bereczki Z., Blattner F. R. ( 1999). Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 27:4409–4415 [View Article][PubMed]
    [Google Scholar]
  114. Qazi S. N., Counil E., Morrissey J., Rees C. E., Cockayne A., Winzer K., Chan W. C., Williams P., Hill P. J. ( 2001a). agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect Immun 69:7074–7082 [View Article][PubMed]
    [Google Scholar]
  115. Qazi S. N., Rees C. E., Mellits K. H., Hill P. J. ( 2001b). Development of gfp vectors for expression in Listeria monocytogenes and other low G+C Gram positive bacteria. Microb Ecol 41:301–309[PubMed]
    [Google Scholar]
  116. Qazi S. N., Harrison S. E., Self T., Williams P., Hill P. J. ( 2004). Real-time monitoring of intracellular Staphylococcus aureus replication. J Bacteriol 186:1065–1077 [View Article][PubMed]
    [Google Scholar]
  117. Redder P., Linder P. ( 2012). New range of vectors with a stringent 5-fluoroorotic acid-based counterselection system for generating mutants by allelic replacement in Staphylococcus aureus . Appl Environ Microbiol 78:3846–3854 [View Article][PubMed]
    [Google Scholar]
  118. Reznikoff W. S. ( 2003). Tn5 as a model for understanding DNA transposition. Mol Microbiol 47:1199–1206 [View Article][PubMed]
    [Google Scholar]
  119. Reznikoff W. S., Bhasin A., Davies D. R., Goryshin I. Y., Mahnke L. A., Naumann T., Rayment I., Steiniger-White M., Twining S. S. ( 1999). Tn5: A molecular window on transposition. Biochem Biophys Res Commun 266:729–734 [View Article][PubMed]
    [Google Scholar]
  120. Sastalla I., Chim K., Cheung G. Y., Pomerantsev A. P., Leppla S. H. ( 2009). Codon-optimized fluorescent proteins designed for expression in low-GC gram-positive bacteria. Appl Environ Microbiol 75:2099–2110 [View Article][PubMed]
    [Google Scholar]
  121. Sauer B. ( 2004). Chromosome manipulation by Cre-lox recombination. Mobile DNA II38–58 Craig N. L., Craigie R., Gellert M., Lambowitz A. M. Washington, DC: ASM Press;
    [Google Scholar]
  122. Schofield D. A., Westwater C., Hoel B. D., Werner P. A., Norris J. S., Schmidt M. G. ( 2003). Development of a thermally regulated broad-spectrum promoter system for use in pathogenic gram-positive species. Appl Environ Microbiol 69:3385–3392 [View Article][PubMed]
    [Google Scholar]
  123. Scholz O., Henßler E.-M., Bail J., Schubert P., Bogdanska-Urbaniak J., Sopp S., Reich M., Wisshak S., Köstner M. & other authors ( 2004). Activity reversal of Tet repressor caused by single amino acid exchanges. Mol Microbiol 53:777–789 [View Article][PubMed]
    [Google Scholar]
  124. Sheehan B. J., Foster T. J., Dorman C. J., Park S., Stewart G. S. ( 1992). Osmotic and growth-phase dependent regulation of the eta gene of Staphylococcus aureus: a role for DNA supercoiling. Mol Gen Genet 232:49–57 [View Article][PubMed]
    [Google Scholar]
  125. Sizemore C., Buchner E., Rygus T., Witke C., Götz F., Hillen W. ( 1991). Organization, promoter analysis and transcriptional regulation of the Staphylococcus xylosus xylose utilization operon. Mol Gen Genet 227:377–384 [View Article][PubMed]
    [Google Scholar]
  126. Sizemore C., Wieland B., Götz F., Hillen W. ( 1992). Regulation of Staphylococcus xylosus xylose utilization genes at the molecular level. J Bacteriol 174:3042–3048[PubMed]
    [Google Scholar]
  127. Southward C. M., Surette M. G. ( 2002). The dynamic microbe: green fluorescent protein brings bacteria to light. Mol Microbiol 45:1191–1196 [View Article][PubMed]
    [Google Scholar]
  128. Stary E., Gaupp R., Lechner S., Leibig M., Tichy E., Kolb M., Bertram R. ( 2010). New architectures for Tet-on and Tet-off regulation in Staphylococcus aureus . Appl Environ Microbiol 76:680–687 [View Article][PubMed]
    [Google Scholar]
  129. Steidler L., Yu W., Fiers W., Remaut E. ( 1996). The expression of the Photinus pyralis luciferase gene in Staphylococcus aureus Cowan I allows the development of a live amplifiable tool for immunodetection. Appl Environ Microbiol 62:2356–2359[PubMed]
    [Google Scholar]
  130. Stewart P. R., Waldron H. G., Lee J. S., Matthews P. R. ( 1985). Molecular relationships among serogroup B bacteriophages of Staphylococcus aureus . J Virol 55:111–116[PubMed]
    [Google Scholar]
  131. Takahashi T., Satoh I., Kikuchi N. ( 1999). Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis. Int J Syst Bacteriol 49:725–728 [View Article][PubMed]
    [Google Scholar]
  132. Terpe K. ( 2006). Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 72:211–222 [View Article][PubMed]
    [Google Scholar]
  133. Topp S., Reynoso C. M., Seeliger J. C., Goldlust I. S., Desai S. K., Murat D., Shen A., Puri A. W., Komeili A. & other authors ( 2010). Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl Environ Microbiol 76:7881–7884 [View Article][PubMed]
    [Google Scholar]
  134. van Kessel J. C., Hatfull G. F. ( 2008). Efficient point mutagenesis in mycobacteria using single-stranded DNA recombineering: characterization of antimycobacterial drug targets. Mol Microbiol 67:1094–1107 [View Article][PubMed]
    [Google Scholar]
  135. van Pijkeren J. P., Britton R. A. ( 2012). High efficiency recombineering in lactic acid bacteria. Nucleic Acids Res 40:e76 [View Article][PubMed]
    [Google Scholar]
  136. Vandenesch F., Kornblum J., Novick R. P. ( 1991). A temporal signal, independent of agr, is required for hla but not spa transcription in Staphylococcus aureus . J Bacteriol 173:6313–6320[PubMed]
    [Google Scholar]
  137. Waldron D. E., Lindsay J. A. ( 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 188:5578–5585 [View Article][PubMed]
    [Google Scholar]
  138. Wang P. Z., Projan S. J., Leason K. R., Novick R. P. ( 1987). Translational fusion with a secretory enzyme as an indicator. J Bacteriol 169:3082–3087[PubMed]
    [Google Scholar]
  139. Wieland K. P., Wieland B., Götz F. ( 1995). A promoter-screening plasmid and xylose-inducible, glucose-repressible expression vectors for Staphylococcus carnosus . Gene 158:91–96 [View Article][PubMed]
    [Google Scholar]
  140. Wittmann A., Suess B. ( 2012). Engineered riboswitches: expanding researchers’ toolbox with synthetic RNA regulators. FEBS Lett 586:2076–2083 [View Article][PubMed]
    [Google Scholar]
  141. Xia M., Lunsford R. D., McDevitt D., Iordanescu S. ( 1999). Rapid method for the identification of essential genes in Staphylococcus aureus . Plasmid 42:144–149 [View Article][PubMed]
    [Google Scholar]
  142. Xu H. H., Trawick J. D., Haselbeck R. J., Forsyth R. A., Yamamoto R. T., Archer R., Patterson J., Allen M., Froelich J. M. & other authors ( 2010). Staphylococcus aureus TargetArray: comprehensive differential essential gene expression as a mechanistic tool to profile antibacterials. Antimicrob Agents Chemother 54:3659–3670 [View Article][PubMed]
    [Google Scholar]
  143. Xu S. Y., Corvaglia A. R., Chan S. H., Zheng Y., Linder P. ( 2011). A type IV modification-dependent restriction enzyme SauUSI from Staphylococcus aureus subsp. aureus USA300. Nucleic Acids Res 39:5597–5610 [View Article][PubMed]
    [Google Scholar]
  144. Yamachika S., Onodera Y., Hiramatsu K., Takase H. ( 2012). Plasmid integration method: a new tool for analysis of the essentiality and function of genes in S. aureus . J Microbiol Methods 90:250–255 [View Article][PubMed]
    [Google Scholar]
  145. Yansura D. G., Henner D. J. ( 1984). Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis . Proc Natl Acad Sci U S A 81:439–443 [View Article][PubMed]
    [Google Scholar]
  146. Yao J., Zhong J., Fang Y., Geisinger E., Novick R. P., Lambowitz A. M. ( 2006). Use of targetrons to disrupt essential and nonessential genes in Staphylococcus aureus reveals temperature sensitivity of Ll.LtrB group II intron splicing. RNA 12:1271–1281 [View Article][PubMed]
    [Google Scholar]
  147. Yu W., Götz F. ( 2012). Cell wall antibiotics provoke accumulation of anchored mCherry in the cross wall of Staphylococcus aureus . PLoS ONE 7:e30076 [View Article][PubMed]
    [Google Scholar]
  148. Zhang Y., Buchholz F., Muyrers J. P., Stewart A. F. ( 1998). A new logic for DNA engineering using recombination in Escherichia coli . Nat Genet 20:123–128 [View Article][PubMed]
    [Google Scholar]
  149. Zhang L., Fan F., Palmer L. M., Lonetto M. A., Petit C., Voelker L. R., St John A., Bankosky B., Rosenberg M., McDevitt D. ( 2000). Regulated gene expression in Staphylococcus aureus for identifying conditional lethal phenotypes and antibiotic mode of action. Gene 255:297–305 [View Article][PubMed]
    [Google Scholar]
  150. Zheng L., Yang J., Landwehr C., Fan F., Ji Y. ( 2005). Identification of an essential glycoprotease in Staphylococcus aureus . FEMS Microbiol Lett 245:279–285 [View Article][PubMed]
    [Google Scholar]
  151. Zoraghi R., See R. H., Gong H., Lian T., Swayze R., Finlay B. B., Brunham R. C., McMaster W. R., Reiner N. E. ( 2010). Functional analysis, overexpression, and kinetic characterization of pyruvate kinase from methicillin-resistant Staphylococcus aureus . Biochemistry 49:7733–7747 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.061705-0
Loading
/content/journal/micro/10.1099/mic.0.061705-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error