Isolation and characterization of biofilm formation-defective mutants of Staphylococcus aureus

Infection and Immunity

Volumn 75, Issue 3, 2007, Pages 1079-1088

  Tu Quoc, Patrick H ^a   Genevaux, Pierre ^b   Pajunen, Maria ^c   Savilahti, Harri ^c,d   Georgopoulos, Costa ^b   Schrenzel, Jacques ^a   Kelley, William L ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BETA LACTAMASE; HELICASE; TEICHOIC ACID; XYLOSE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIOPHAGE MU; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOFILM; CLONE; CODY GENE; CONTROLLED STUDY; FMTA GENE; GENE CONTROL; GENE DISRUPTION; GENE INSERTION; GENE LOCUS; GENE MAPPING; IMMUNOBLOTTING; MGRA GENE; MORBIDITY; MORTALITY; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FAMILY; PROTEIN MOTIF; SRRA GENE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; VALIDATION PROCESS; WILD TYPE;

BIOFILMS; DNA TRANSPOSABLE ELEMENTS; MUTAGENESIS, INSERTIONAL; STAPHYLOCOCCUS AUREUS;

EID: 33847706577     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01143-06     Document Type: Article

References (79)

1. Becker, P., W. Hufnagle, G. Peters, and M. Herrmann. 2001. Detection of differential gene expression in biofilm-forming versus planktonic populations of Staphylococcus aureus using micro-representational difference analysis. Appl. Environ. Microbiol. 67:2958-2965.
2. Beenken, K. E., P. M. Dunman, F. McAleese, D. Macapagal, E. Murphy, S. J. Projan, J. S. Blevins, and M. S. Smeltzer. 2004. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186:4665-4684.
3. Brouillette, E., M. Hyodo, Y. Hayakawa, D. K. R. Karaolis, and F. Malmouin. 2005. 3′-5′-cyclic diguanylic acid reduces the virulence of biofilm-forming Staphylococcus aureus strains in a mouse model of mastitis infection. Antimicrobial. Agents Chemother. 49:3109-3113.
4. Callebaut, I., D. Moshous, J.-P. Mornon, and J.-P. de Villartay. 2002. Metallo-β-lactamases fold within nucleic acids processing enzymes: the β-CASP family. Nucleic Acids Res. 30:3592-3601.
5. Campbell, T. L., J. Henderson, D. E. Heinrichs, and E. D. Brown. 2006. The yjeQ gene is required for virulence of Staphylococcus aureus. Infect. Immun. 74:4918-4921.
6. Conlon, K. M., H. Humphreys, and J. P. O'Gara. 2002. Regulation of icaR gene expression in Staphylococcus epidermidis. FEMS Microbiol. Lett. 216: 171-177.
7. Conlon, K. M., H. Humphreys, and J. P. O'Gara. 2002. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J. Bacteriol. 184:4400-4408.
8. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
9. Cramton, S. E., C. Gerke, N. F. Schnell, W. W. Nichols, and F. Götz. 1999. The intercellular adhesin (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
10. Cramton, S. E., M. Ulrich, F. Götz, and G. Doring. 2001. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69:4079-4085.
11. Cucarella, C., C. Solano, J. Valle, B. Amorena, I. Lasa, and J. R. Penadés. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896.
12. Daigle, D. M., L. Rossi, A. M. Berghuis, L. Aravind, E. V. Koonin, and E. D. Brown. 2002. YjeQ, an essential, conserved, uncharacterized protein from Escherichia coli, is an unusual GTPase with circularly permuted G-motifs and marked burst kinetics. Biochemistry 41:11109-11117.
13. Deighton, M., and R. Borland. 1993. Regulation of slime production in Staphylococcus epidermidis by iron limitation. Infect. Immun. 61:4473-4479.
14. Dobinsky, S., K. Kiel, H. Rohde, K. Bartscht, J. K. Knobloch, M. A. Horstkotte, and D. Mack. 2003. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J. Bacteriol. 185: 2879-2886.
15. Fitzpatrick, F., H. Humphrey, and J. P. O'Gara. 2005. The genetics of staphylococcal biofilm formation-will a greater understanding of pathogenesis lead to better management of device-related infection? Clin. Microbiol. Infect. 11:967-973.
16. Fluckiger, U., M. Ulrich, A. Steinhuber, G. Doring, D. Mack, R. Landmann, C. Goerke, and C. Wol. 2005. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect. Immun. 73:1811-1819.
17. Fux, C. A., J. W. Costerton, P. S. Stewart, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:34-40.
18. Gerke, C., A. Kraft, R. Süssmuth, O. Schweitzer, and F. Götz. 1998. Characterization of the N-acetylglucosaminyl-transferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesion. J. Biol. Chem. 273:18586-18593.
19. Götz, F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43:1367-1378.
20. Gross, M., S. E. Cramton, F. Götz, and A. Peschel. 2001. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69:3423-3426.
21. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108.
22. Heilmann, C., C. Gerke, F. Perdreau-Remington, and F. Götz. 1996. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun. 64:277-282.
23. Heilmann, C., O. Schweitzer, C. Gerke, N. Vanittanakom, D. Mack, and F. Götz. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20:1083-1091.
24. Heilmann, C., M. Hussain, G. Peters, and F. Götz. 1997. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol. 24:1013-1024.
25. Hickman, J. W., D. F. Tifrea, and C. S. Harwood. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102:14422-14427.
26. Ingavale, S. S., W. Van Wamel, and A. L. Cheung. 2003. Characterization of RAT, an autolysis regulator in Staphylococcus aureus. Mol. Microbiol. 48: 1451-1466.
27. Jefferson, K. K., D. B. Pier, D. A. Goldmann, and G. B. Pier. 2004. The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesion locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. J. Bacteriol. 186:2449-2456.
28. Jenal, U. 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7:185-191.
29. Johnson, M., A. Cockayne, P. H. Williams, and J. A. Morrissey. 2005. Iron-responsive regulation of biofilm formation in Staphylococcus aureus involves Fur-dependent and Fur-independent mechanisms. J. Bacteriol. 187: 8211-8215.
30. Karaolis, D. K. R., M. H. Rashid, R. Chythanya, W. Luo, M. Hyodo, and Y. Hayakawa. 2005. c-di-GMP (3′-5′-cyclic diguanylic acid) inhibits Staphylococcus aureus cell-cell interactions and biofilm formation. Antimicrob. Agents Chemother. 49:1029-1038.
31. Kim, L., A. Mogk, and W. Schumann. 1996. A xylose-inducible Bacillus subtilis integration vector and its application. Gene 181:71-76.
32. B by repression of the negative regulator gene icaR. Infect. Immun. 72:3838-3848.
33. Komatsuzawa, H., K. Ohta, H. Labishinski, M. Sugai, and H. Suginaka. 1999. Characterization of fmtA, a gene that modulates the expression of methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 43:2121-2125.
34. Kreiswirth, B. N., S. Lofdahl, M. J. Betley, M. O'Reilly, P. M. Schlievert, M. S. Bergdoll, and R. P. Novick. 1983. The toxic shock syndrome exotoxin structural gene is not detectable transmitted by a prophage. Nature 305:709-712.
35. Kropec, A., T. Maira-Litrán, K. K. Jefferson, M. Grout, S. E. Cramton, F. Götz, D. A. Goldmann, and G. B. Pier. 2005. Poly N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect. Immun. 73:6868-6876.
36. Lamberg, A., S. Nieminen, M. Qiao, and H. Savilahti. 2002. Efficient insertion mutagenesis strategy for bacterial genomes involving electroporation of in vitro-assembled DNA transposition complexes of bacteriophage mu. Appl. Environ. Microbiol. 68:705-712.
37. Lasa, I., and J. Penadés. 2006. Bap: a family of surface proteins involved in biofilm formation. Res. Microbiol. 157:99-107.
38. Lazarevic, V., and D. Karamata. 1995. The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol. Microbiol. 16:345-355.
39. Lee, J. C. 1995. Electroporation of staphylococci. Methods Mol. Biol. 47: 209-216.
40. Lew, D. P., and F. A. Waldvogel. 2004. Osteomyelitis. Lancet 364:369-379.
41. Ljungh, A., S. Hjerton, and T. T. Wadstrom. 1985. High surface hydrophobicity of autoaggregating Staphylococcus aureus strains isolated from human infections studied with the salt aggregation test. Infect. Immun. 47:522-526.
42. Luong, T. T., S. W. Newell, and C. Y. Lee. 2003. Mgr, a novel global regulator in Staphylococcus aureus. J. Bacteriol. 185:3703-3710.
43. Mack, D., N. Siemssen, and R. Laufs. 1992. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect. Immun. 60:2048-2057.
44. Mack, D., M. Nedelmann, A. Krokotsch, A. Schwartzkopf, J. Heesemann, and R. Laufs. 1994. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesion. Infect. Immun. 62:3244-3253.
45. Mack, D., M. Haeder, N. Siemssen, and R. Laufs. 1996. Association of biofilm production of coagulase-negative staphylococci with expression of a specific polysaccharide intercellular adhesion. J. Infect. Dis. 174:881-584.
46. Mah, T.-F. C., and G. A. O'Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39.
47. Maira-Litrán, T., A. Kropec, C. Abeygunawardana, J. Joyce, G. Mark, D. A. Goldmann, and G. B. Pier. 2002. Immunochemical properties of staphylococcal poly N-acetylglucosamine surface polysaccharide. Infect. Immun. 70: 4433-4440.
48. Maki, H., T. Yamaguchi, and K. Murakami. 1994. Cloning and characterization of a gene affecting the methicillin resistance level and autolysis rate in Staphylococcus aureus. J. Bacteriol. 176:4993-5000.
49. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429-1449.
50. Pajunen, M. I., A. T. Pullianen, J. Finne, and H. Savilahti. 2005. Generation of transposon insertion mutant libraries for gram-positive bacteria by electroporation of phage Mu DNA transposition complexes. Microbiology 151: 1209-1218.
51. Pao, S. S., I. T. Paulsen, and M. H. Saier. 1998. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62:1-34.
52. Park, S. F., and G. S. Stewart. 1990. High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94:129-132.
53. Parsek, M. R., and P. K. Singh. 2003. Bacterial biofilms: and emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701.
54. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274: 8405-8410.
55. Pragman, A. A., J. M. Yarwood, T. T. Tripp, and P. M. Schlievert. 2004. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. J. Bacteriol. 186:2430-2438.
56. B is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J. Bacteriol. 182:6824-6826.
57. Resch, A., R. Resenstein, C. Nerz, and F. Götz. 2005. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 71:2663-2676.
58. Resch, A., S. Leicht, M. Saric, L. Pasztor, A. Jakob, F. Götz, and A. Nordheim. 2006. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6:1867-1877.
59. Rocak, S., and P. Linder. 2004. DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5:232-241.
60. Rohde, H., C. Burdelski, K. Bartscht, M. Hussain, F. Buck, M. A. Horstkotte, J. K.-M. Knobloch, C. Heilmann, M. Hermann, and D. Mack. 2005. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol. 55:1883-1895.
61. Roos, S., S. Lindgren, and H. Jonsson. 1999. Autoaggregation of Lactobacillus reuteri is mediated by a putative DEAD box helicase. Mol. Microbiol. 32:427-436.
62. Rupp, M. E., J. S. Ulphani, P. D. Few, K. Bartscht, and D. Mack. 1999. Characterization of the importance of polysaccharide intercellular adhesion/ hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect. Immun. 67:2627-2632.
63. Shanks, R. M., N. P. Donegan, M. L. Graber, S. E. Buckingham, M. E. Zegans, A. L. Cheung, and G. A. O'Toole. 2005. Heparin stimulates Staphylococcus aureus biofilm formation. Infect. Immun. 73:4596-4606.
64. Shirtliff, M. E., J. T. Mader, and A. K. Camper. 2002. Molecular interactions in biofilms. Chem. Biol. 9:859-871.
65. Sonenshein, A. L. 2005. CodY, a global regulator of stationary phase and virulence in gram-positive bacteria. Curr. Opin. Microbiol. 8:203-207.
66. Throup, J. P., F. Zappacosta, R. D. Lunsford, R. S. Annan, S. A. Carr, J. T. Lonsdale, A. P. Bryant, D. McDevitt, M. Rosenberg, and M. K. R. Burnham. 2001. The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry 40:10392-10401.
67. Toledo-Arana, A., N. Merino, M. Vergara-Irigaray, M. Débarbouillé, J. R. Penadés, and I. Lasa. 2005. Staphylococcus aureus develops an alternative, ice-independent biofilm in the absence of the arlRS two-component system. J. Bacteriol. 187:5318-5329.
68. Tormo, M. A., M. Martí, J. Valle, A. C. Manna, A. L. Cheung, I. Lasa, and J. R. Penades. 2005. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J. Bacteriol. 187:2348-2356.
69. Truong-Bolduc, Q. C., X. Zhang, and D. C. Hooper. 2003. Characterization of NorR protein, a multifunctional regulator of norA expression in Staphylococcus aureus. J. Bacteriol. 185:3127-3138.
70. B is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48:1075-1087.
71. B. J. Bacteriol. 175:3964-3971.
72. Vuong, C., H. L. Saenz, F. Götz, and M. Otto. 2000. Impact of the agr quorum sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182:1688-1693.
73. Vuong, C., J. B. Kidder, E. R. Jacobson, M. Otto, R. A. Proctor, and G. A. Somerville. 2005. Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. J. Bacteriol. 187:2967-2973.
74. Wang, L., J. D. Trawick, R. Yamamoto, and C. Zamudio. 2004. Genomewide operon prediction in Staphylococcus aureus. Nucleic Acids Res. 32: 3689-3702.
75. Weidenmaier, C., J. F. Kokai-Kun, S. A. Kristian, T. Chanturiya, H. Kalbacher, M. Gross, G. Nicholson, B. Neumeister, J. J. Mond, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-2445.
76. Wolters, P. J., K. M. Hildebrandt, J. P. Dickie, and J. S. Anderson. 1990. Polymer length of teichuronic acid released from cell walls of Micrococcus luteus. J. Bacteriol. 172:5154-5515.
77. Xu, L., H. Li, C. Vuong, V. Vadyvaloo, J. Wang, Y. Yao, M. Otto, and Q. Gao. 2006. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect. Immun. 74:488-496.
78. Yao, Y., D. E. Sturderant, and M. Otto. 2005. Genome wide analysis of gene expression in Staphylococcus epidermidis biofilms: insights in the the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis. 191:289-298.
79. Yarwood, J. M., J. K. McCormick, and P. Schlievert. 2001. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 183:1113-1123.