1887

Abstract

In ocular infections (OIs) caused by , biofilms composed mainly of poly--acetylglucosamine (PNAG) have been widely studied, but PNAG-independent biofilms have not. Therefore, we searched for a relationship between the operon (involved in PNAG-biofilm) and the biochemical composition of biofilms in isolates from OI. Isolates from OI ( = 62), from healthy conjunctiva (HC;  = 45) and from healthy skin (HS;  = 53), were used to detect and genes, and the insertion sequence 256 (IS) using PCR. The compositions of the biofilms were determined by treatment with NaIO, proteinase K and DNase I. Multilocus sequence typing (MLST) was performed to characterize the isolates, and the expression of and genes was determined by real-time qPCR. A strong relationship between the / /IS genotype and protein- or protein/extracellular DNA (eDNA)-biofilm composition was found in the isolates from OI (53.6 %), whereas the / /IS genotype and carbohydrate-biofilm was most prevalent in isolates from HC (25 %) and HS (25 %). Isolates with an / /IS genotype and protein-biofilm phenotype were predominantly of the ST2 lineage, while carbohydrate-biofilm-producing strains were mainly of the ST9 lineage. The protein-biofilm-producing strains had higher expression levels of gene than carbohydrate-biofilm-producing strains; while gene did not have the same pattern of expression. These results suggest that strains with //IS genotype and protein- or protein/eDNA-biofilms have a stronger ability to establish in the eye than strains with //IS genotype and PNAG-biofilms.

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2013-10-01
2019-12-06
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References

  1. Arrecubieta C. , Lee M. H. , Macey A. , Foster T. J. , Lowy F. D. . ( 2007; ). SdrF, a Staphylococcus epidermidis surface protein, binds type I collagen. . J Biol Chem 282:, 18767–18776. [CrossRef] [PubMed]
    [Google Scholar]
  2. Baillif S. , Ecochard R. , Casoli E. , Freney J. , Burillon C. , Kodjikian L. J. . ( 2008; ). Adherence and kinetics of biofilm formation of Staphylococcus epidermidis to different types of intraocular lenses under dynamic flow conditions. . J Cataract Refract Surg 34:, 153–158. [CrossRef] [PubMed]
    [Google Scholar]
  3. Banner M. A. , Cunniffe J. G. , Macintosh R. L. , Foster T. J. , Rohde H. , Mack D. , Hoyes E. , Derrick J. , Upton M. , Handley P. S. . ( 2007; ). Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. . J Bacteriol 189:, 2793–2804. [CrossRef] [PubMed]
    [Google Scholar]
  4. Catalanotti P. , Lanza M. , Del Prete A. , Lucido M. , Catania M. R. , Gallè F. , Boggia D. , Perfetto B. , Rossano F. . ( 2005; ). Slime-producing Staphylococcus epidermidis and S. aureus in acute bacterial conjunctivitis in soft contact lens wearers. . New Microbiol 28:, 345–354.[PubMed]
    [Google Scholar]
  5. Christensen G. D. , Simpson W. A. , Younger J. J. , Baddour L. M. , Barrett F. F. , Melton D. M. , Beachey E. H. . ( 1985; ). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. . J Clin Microbiol 22:, 996–1006.[PubMed]
    [Google Scholar]
  6. Christner M. , Franke G. C. , Schommer N. N. , Wendt U. , Wegert K. , Pehle P. , Kroll G. , Schulze C. , Buck F. . & other authors ( 2010; ). The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. . Mol Microbiol 75:, 187–207. [CrossRef] [PubMed]
    [Google Scholar]
  7. Conlan S. , Mijares L. A. , NISC Comparative Sequencing Program, , Becker J. , Blakesley R. W. , Bouffard G. G. , Brooks S. , Coleman H. , Gupta J. . & other authors ( 2012; ). Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. . Genome Biol 13:, R64. [CrossRef] [PubMed]
    [Google Scholar]
  8. Conlon K. M. , Humphreys H. , O’Gara J. P. . ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  9. Conrad A. , Suutari M. K. , Keinänen M. M. , Cadoret A. , Faure P. , Mansuy-Huault L. , Block J. C. . ( 2003; ). Fatty acids of lipid fractions in extracellular polymeric substances of activated sludge flocs. . Lipids 38:, 1093–1105. [CrossRef] [PubMed]
    [Google Scholar]
  10. Costerton J. W. , Stewart P. S. , Greenberg E. P. . ( 1999; ). Bacterial biofilms: a common cause of persistent infections. . Science 284:, 1318–1322. [CrossRef] [PubMed]
    [Google Scholar]
  11. Cue D. , Lei M. G. , Luong T. T. , Kuechenmeister L. , Dunman P. M. , O’Donnell S. , Rowe S. , O’Gara J. P. , Lee C. Y. . ( 2009; ). Rbf promotes biofilm formation by Staphylococcus aureus via repression of icaR, a negative regulator of icaADBC. . J Bacteriol 191:, 6363–6373. [CrossRef] [PubMed]
    [Google Scholar]
  12. Duggirala A. , Kenchappa P. , Sharma S. , Peeters J. K. , Ahmed N. , Garg P. , Das T. , Hasnain S. E. . ( 2007; ). High-resolution genome profiling differentiated Staphylococcus epidermidis isolated from patients with ocular infections and normal individuals. . Invest Ophthalmol Vis Sci 48:, 3239–3245. [CrossRef] [PubMed]
    [Google Scholar]
  13. Frølund B. , Palmgren R. , Keiding K. , Nielsen P. H. . ( 1996; ). Extraction of extracellular polymers from activated sludge using a cation exchange resin. . Water Res 30:, 1749–1758. [CrossRef]
    [Google Scholar]
  14. Gerke C. , Kraft A. , Süssmuth R. , Schweitzer O. , Götz F. . ( 1998; ). Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. . J Biol Chem 273:, 18586–18593. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hartford O. , O’Brien L. , Schofield K. , Wells J. , Foster T. J. . ( 2001; ). The Fbe (SdrG) protein of Staphylococcus epidermidis HB promotes bacterial adherence to fibrinogen. . Microbiology 147:, 2545–2552.[PubMed]
    [Google Scholar]
  16. Heilmann C. , Schweitzer O. , Gerke C. , Vanittanakom N. , Mack D. , Götz F. . ( 1996; ). Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. . Mol Microbiol 20:, 1083–1091. [CrossRef] [PubMed]
    [Google Scholar]
  17. Heilmann C. , Hussain M. , Peters G. , Götz F. . ( 1997; ). Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. . Mol Microbiol 24:, 1013–1024. [CrossRef] [PubMed]
    [Google Scholar]
  18. Heilmann C. , Thumm G. , Chhatwal G. S. , Hartleib J. , Uekötter A. , Peters G. . ( 2003; ). Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. . Microbiology 149:, 2769–2778. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hussain M. , Herrmann M. , von Eiff C. , Perdreau-Remington F. , Peters G. A. . ( 1997; ). A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces. . Infect Immun 65:, 519–524.[PubMed]
    [Google Scholar]
  20. Izano E. A. , Amarante M. A. , Kher W. B. , Kaplan J. B. . ( 2008; ). Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. . Appl Environ Microbiol 74:, 470–476. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jefferson K. K. , Pier D. B. , Goldmann D. A. , Pier G. B. . ( 2004; ). The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. . J Bacteriol 186:, 2449–2456. [CrossRef] [PubMed]
    [Google Scholar]
  22. Juárez-Verdayes M. A. , Reyes-López M. A. , Cancino-Díaz M. E. , Muñoz-Salas S. , Rodríguez-Martínez S. , de la Serna F. J. , Hernández-Rodríguez C. H. , Cancino-Díaz J. C. . ( 2006; ). Isolation, vancomycin resistance and biofilm production of Staphylococcus epidermidis from patients with conjunctivitis, corneal ulcers, and endophthalmitis. . Rev Latinoam Microbiol 48:, 238–246.[PubMed]
    [Google Scholar]
  23. Kogan G. , Sadovskaya I. , Chaignon P. , Chokr A. , Jabbouri S. . ( 2006; ). Biofilms of clinical strains of Staphylococcus that do not contain polysaccharide intercellular adhesin. . FEMS Microbiol Lett 255:, 11–16. [CrossRef] [PubMed]
    [Google Scholar]
  24. Kozitskaya S. , Cho S. H. , Dietrich K. , Marre R. , Naber K. , Ziebuhr W. . ( 2004; ). The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides. . Infect Immun 72:, 1210–1215. [CrossRef] [PubMed]
    [Google Scholar]
  25. Li M. , Wang X. , Gao Q. , Lu Y. . ( 2009; ). Molecular characterization of Staphylococcus epidermidis strains isolated from a teaching hospital in Shanghai, China. . J Med Microbiol 58:, 456–461. [CrossRef] [PubMed]
    [Google Scholar]
  26. Macintosh R. L. , Brittan J. L. , Bhattacharya R. , Jenkinson H. F. , Derrick J. , Upton M. , Handley P. S. . ( 2009; ). The terminal A domain of the fibrillar accumulation-associated protein (Aap) of Staphylococcus epidermidis mediates adhesion to human corneocytes. . J Bacteriol 191:, 7007–7016. [CrossRef] [PubMed]
    [Google Scholar]
  27. Mack D. , Fischer W. , Krokotsch A. , Leopold K. , Hartmann R. , Egge H. , Laufs R. . ( 1996; ). The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear β-1,6-linked glucosaminoglycan: purification and structural analysis. . J Bacteriol 178:, 175–183.[PubMed]
    [Google Scholar]
  28. National Nosocomial Infections Surveillance System ( 2004; ). National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. . Am J Infect Control 32:, 470–485. [CrossRef] [PubMed]
    [Google Scholar]
  29. Pamp S. J. , Frees D. , Engelmann S. , Hecker M. , Ingmer H. . ( 2006; ). Spx is a global effector impacting stress tolerance and biofilm formation in Staphylococcus aureus. . J Bacteriol 188:, 4861–4870. [CrossRef] [PubMed]
    [Google Scholar]
  30. Patel J. D. , Colton E. , Ebert M. , Anderson J. M. . ( 2012; ). Gene expression during S. epidermidis biofilm formation on biomaterials. . J Biomed Mater Res A 100:, 2863–2869.[PubMed] [CrossRef]
    [Google Scholar]
  31. Ravaioli S. , Campoccia D. , Visai L. , Pirini V. , Cangini I. , Corazzari T. , Maso A. , Poggio C. , Pegreffi F. . & other authors ( 2011; ). Biofilm extracellular-DNA in 55 Staphylococcus epidermidis clinical isolates from implant infections. . Int J Artif Organs 34:, 840–846. [CrossRef] [PubMed]
    [Google Scholar]
  32. Rice K. C. , Mann E. E. , Endres J. L. , Weiss E. C. , Cassat J. E. , Smeltzer M. S. , Bayles K. W. . ( 2007; ). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. . Proc Natl Acad Sci U S A 104:, 8113–8118. [CrossRef] [PubMed]
    [Google Scholar]
  33. Rohde H. , Burdelski C. , Bartscht K. , Hussain M. , Buck F. , Horstkotte M. A. , Knobloch J. K. , Heilmann C. , Herrmann M. , Mack D. . ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rohde H. , Burandt E. C. , Siemssen N. , Frommelt L. , Burdelski C. , Wurster S. , Scherpe S. , Davies A. P. , Harris L. G. . & other authors ( 2007; ). Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. . Biomaterials 28:, 1711–1720. [CrossRef] [PubMed]
    [Google Scholar]
  35. Ryder C. , Byrd M. , Wozniak D. J. . ( 2007; ). Role of polysaccharides in Pseudomonas aeruginosa biofilm development. . Curr Opin Microbiol 10:, 644–648. [CrossRef] [PubMed]
    [Google Scholar]
  36. Suzuki T. , Kawamura Y. , Uno T. , Ohashi Y. , Ezaki T. . ( 2005; ). Prevalence of Staphylococcus epidermidis strains with biofilm-forming ability in isolates from conjunctiva and facial skin. . Am J Ophthalmol 140:, 844–850, 850.e1. [CrossRef] [PubMed]
    [Google Scholar]
  37. Thomas J. C. , Vargas M. R. , Miragaia M. , Peacock S. J. , Archer G. L. , Enright M. C. . ( 2007; ). Improved multilocus sequence typing scheme for Staphylococcus epidermidis. . J Clin Microbiol 45:, 616–619. [CrossRef] [PubMed]
    [Google Scholar]
  38. Tormo M. A. , Knecht E. , Götz F. , Lasa I. , Penadés J. R. . ( 2005; ). Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer?. Microbiology 151:, 2465–2475. [CrossRef] [PubMed]
    [Google Scholar]
  39. Ulrich M. , Bastian M. , Cramton S. E. , Ziegler K. , Pragman A. A. , Bragonzi A. , Memmi G. , Wolz C. , Schlievert P. M. . & other authors ( 2007; ). The staphylococcal respiratory response regulator SrrAB induces ica gene transcription and polysaccharide intercellular adhesin expression, protecting Staphylococcus aureus from neutrophil killing under anaerobic growth conditions. . Mol Microbiol 65:, 1276–1287. [CrossRef] [PubMed]
    [Google Scholar]
  40. Vacheethasanee K. , Temenoff J. S. , Higashi J. M. , Gary A. , Anderson J. M. , Bayston R. , Marchant R. E. . ( 1998; ). Bacterial surface properties of clinically isolated Staphylococcus epidermidis strains determine adhesion on polyethylene. . J Biomed Mater Res 42:, 425–432. [CrossRef] [PubMed]
    [Google Scholar]
  41. Vaningelgem F. , Zamfir M. , Mozzi F. , Adriany T. , Vancanneyt M. , Swings J. , De Vuyst L. . ( 2004; ). Biodiversity of exopolysaccharides produced by Streptococcus thermophilus strains is reflected in their production and their molecular and functional characteristics. . Appl Environ Microbiol 70:, 900–912. [CrossRef] [PubMed]
    [Google Scholar]
  42. Vuong C. , Kocianova S. , Voyich J. M. , Yao Y. , Fischer E. R. , DeLeo F. R. , Otto M. . ( 2004; ). A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. . J Biol Chem 279:, 54881–54886. [CrossRef] [PubMed]
    [Google Scholar]
  43. Ziebuhr W. , Krimmer V. , Rachid S. , Lössner I. , Götz F. , Hacker J. . ( 1999; ). A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256 . . Mol Microbiol 32:, 345–356. [CrossRef] [PubMed]
    [Google Scholar]
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