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Volume 64, Issue 6

Effects of erythromycin on the phenotypic and genotypic biofilm expression in two clinical subspecies and a functional analysis of Ica proteins in Free

Abstract

The operon encoding polysaccharide intercellular adhesion, which facilitates biofilm formation in staphylococci, has been extensively studied in and . Based on analysis, we suggest the following functional model for Ica proteins in IcaA is responsible for polysaccharide synthesis. IcaA and IcaD complete transferring the growing sugar chain to the cell surface; IcaB is a deacetylase, with the same function as IcaB of . IcaC mainly modifies the synthesized glucan by acetylation. We also examined the effects of subinhibitory concentrations of erythromycin on phenotypic biofilm expression and transcription of biofilm-related genes, using isolates representing the two subspecies of and different biofilm and resistance phenotypes. On induction with erythromycin, biofilm density was strongly elevated in two erythromycin-resistant , but not in three susceptible isolates. In the representative erythromycin-resistant subsp. , there were significant upregulations of the gene and its positive regulator on transition to the stationary phase without erythromycin induction. There were also significant increases in the transcription levels of , and corresponding to a very strong biofilm phenotype in the stationary phase on erythromycin stress. In contrast, the representative erythromycin-susceptible subsp. displayed upregulation only of on entry into the stationary phase with erythromycin induction, but this change was not associated with enhancement of biofilm production. These findings suggest that the two subspecies of adopt different pathogenesis and survival strategies to adapt to a hostile environment.

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  • Accepted:
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© 2015 The Authors

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An erratum has been published for this content:
Effects of erythromycin on the phenotypic and genotypic biofilm expression in two clinical subspecies and a functional analysis of Ica proteins in
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2015-06-01
2024-04-24
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References

  1. Baltch A. L., Smith R. P., Franke M. A., Michelsen P. B. 1998; Antibacterial effects of levofloxacin, erythromycin, and rifampin in a human monocyte system against Legionella pneumophila . Antimicrob Agents Chemother 42:3153–3156[PubMed]
     [Google Scholar]
  2. Bannerman T. L., Kloos W. E. 1991; Staphylococcus capitis subsp. ureolyticus subsp. nov. from human skin. Int J Syst Bacteriol 41:144–147 [View Article][PubMed]
     [Google Scholar]
  3. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S. 2004; Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795 [View Article][PubMed]
     [Google Scholar]
  4. Bera A., Herbert S., Jakob A., Vollmer W., Götz F. 2005; Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus . Mol Microbiol 55:778–787 [View Article][PubMed]
     [Google Scholar]
  5. Bernardo K., Pakulat N., Fleer S., Schnaith A., Utermöhlen O., Krut O., Müller S., Krönke M. 2004; Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrob Agents Chemother 48:546–555 [View Article][PubMed]
     [Google Scholar]
  6. Bischoff M., Entenza J. M., Giachino P. 2001; Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus . J Bacteriol 183:5171–5179 [View Article][PubMed]
     [Google Scholar]
  7. Chien Y., Manna A. C., Projan S. J., Cheung A. L. 1999; SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J Biol Chem 274:5237169–37176 [CrossRef]
     [Google Scholar]
  8. 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]
  9. Coelho L. R., Souza R. R., Ferreira F. A., Guimarães M. A., Ferreira-Carvalho B. T., Figueiredo A. M. S. 2008; agr RNAIII divergently regulates glucose-induced biofilm formation in clinical isolates of Staphylococcus aureus . Microbiology 154:113480–3490 [CrossRef]
     [Google Scholar]
  10. Cotter J. J., O'Gara J. P., Mack D., Casey E. 2009; Oxygen-mediated regulation of biofilm development is controlled by the alternative sigma factor σ B in Staphylococcus epidermidis . Appl Environ Microbiol 75:261–264 [View Article][PubMed]
     [Google Scholar]
  11. Cramton S. E., Gerke C., Schnell N. F., Nichols W. W., Götz F. 1999; The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427–5433[PubMed]
     [Google Scholar]
  12. Cui B., Smooker P. M., Rouch D. A., Daley A. J., Deighton M. A. 2013; Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J Clin Microbiol 51:9–14 [View Article][PubMed]
     [Google Scholar]
  13. Cummins J., Reen F. J., Baysse C., Mooij M. J., O'Gara F. 2009; Subinhibitory concentrations of the cationic antimicrobial peptide colistin induce the pseudomonas quinolone signal in Pseudomonas aeruginosa . Microbiology 155:2826–2837 [View Article][PubMed]
     [Google Scholar]
  14. Deighton M. A., Capstick J., Domalewski E., Van Nguyen T. 2001; Methods for studying biofilms produced by Staphylococcus epidermidis . Methods Enzymol 336:177–195[PubMed] [CrossRef]
     [Google Scholar]
  15. Deloménie C., Goodfellow G. H., Krishnamoorthy R., Grant D. M., Dupret J. M. 1997; Study of the role of the highly conserved residues Arg9 and Arg64 in the catalytic function of human N-acetyltransferases NAT1 and NAT2 by site-directed mutagenesis. Biochem J 323:207–215[PubMed]
     [Google Scholar]
  16. Dobinsky S., Kiel K., Rohde H., Bartscht K., Knobloch J. K.-M., Horstkotte M. A., Mack D. 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 [View Article][PubMed]
     [Google Scholar]
  17. Duquenne M., Fleurot I., Aigle M., Darrigo C., Borezée-Durant E., Derzelle S., Bouix M., Deperrois-Lafarge V., Delacroix-Buchet A. 2010; Tool for quantification of staphylococcal enterotoxin gene expression in cheese. App Environ Microbio l76:51367–1374 [CrossRef]
     [Google Scholar]
  18. Drancourt M., Raoult D. 2002; rpoB Gene sequence-based identification of Staphylococcus Species. J Clil Microbiol 40:41333–1338 [CrossRef]
     [Google Scholar]
  19. Gerke C., Kraft A., Süßmuth R., Schweitzer O., Götz F. 1998; Characterization of then-acetylglucosaminyl transferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273:2918586–18593 [CrossRef]
     [Google Scholar]
  20. Götz F. 2002; Staphylococcus and biofilms. Mol Microbiol 43:1367–1378 [View Article][PubMed]
     [Google Scholar]
  21. Govindasamy L., Pedersen B., Lian W., Kukar T., Gu Y., Jin S., Agbandje-McKenna M., Wu D., McKenna R. 2004; Structural insights and functional implications of choline acetyltransferase. J Struct Biol 148:226–235 [View Article][PubMed]
     [Google Scholar]
  22. Heilmann C., Gerke C., Perdreau-Remington F., Götz F. 1996; Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 64:277–282[PubMed]
     [Google Scholar]
  23. Jeng W. Y., Ko T. P., Liu C. I., Guo R. T., Liu C. L., Shr H. L., Wang A. H. 2008; Crystal structure of IcaR, a repressor of the TetR family implicated in biofilm formation in Staphylococcus epidermidis . Nucleic Acids Res 36:51567–1577 [CrossRef]
     [Google Scholar]
  24. Knobloch J. K., Bartscht K., Sabottke A., Rohde H., Feucht H. H., Mack D. 2001; Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J Bacteriol 183:2624–2633 [View Article][PubMed]
     [Google Scholar]
  25. Knobloch J. K.-M., Jäger S., Horstkotte M. A., Rohde H., Mack D. 2004; RsbU-dependent regulation of Staphylococcus epidermidis biofilm formation is mediated via the alternative sigma factor σ B by repression of the negative regulator gene icaR . Infect Immun 72:3838–3848 [View Article][PubMed]
     [Google Scholar]
  26. Lee H. J., Rakić B., Gilbert M., Wakarchuk W. W., Withers S. G., Strynadka N. C. 2009; Structural and kinetic characterizations of the polysialic acid O-acetyltransferase OatWY from Neisseria meningitidis . J Biol Chem 284:24501–24511 [View Article][PubMed]
     [Google Scholar]
  27. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. Methods 25:402–408 [View Article][PubMed]
     [Google Scholar]
  28. Morgan J. L., Strumillo J., Zimmer J. 2013; Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–186 [View Article][PubMed]
     [Google Scholar]
  29. Nalmas S., Bishburg E., Meurillio J., Khoobiar S., Cohen M. 2008; Staphylococcus capitis prosthetic valve endocarditis: report of two rare cases and review of literature. Heart Lung 37:380–384 [View Article][PubMed]
     [Google Scholar]
  30. Ng P. C., Chow V. C. Y., Lee C. H., Ling J. M. L., Wong H. L., Chan R. C. Y. 2006; Persistent Staphylococcus capitis septicemia in a preterm infant. Pediatr Infect Dis J 25:652–654 [View Article][PubMed]
     [Google Scholar]
  31. Nielsen J. S., Christiansen M. H., Bonde M., Gottschalk S., Frees D., Thomsen L. E., Kallipolitis B. H. 2011; Searching for small σ B-regulated genes in Staphylococcus aureus . Arch Microbiol 193:23–34 [View Article][PubMed]
     [Google Scholar]
  32. O'Gara J. P. 2007; ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus . FEMS Microbiol Lett 270:179–188 [View Article][PubMed]
     [Google Scholar]
  33. Picard F. 2004; Use of tuf sequences for genus-specific PCR detection and phylogenetic analysis of 28 streptococcal species. J Clin Microbiol 42:83686–3695 [CrossRef]
     [Google Scholar]
  34. Qiagen 2010; Critical Factors for Successful Real-Time PCR. https://www.qiagen.com/gb/resources/resourcedetail?id = f7efb4f4-fbcf-4b25-9315-c4702414e8d6&lang = en
  35. Qin Z., Ou Y., Yang L., Zhu Y., Tolker-Nielsen T., Molin S., Qu D. 2007; Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis . Microbiology 153:2083–2092 [View Article][PubMed]
     [Google Scholar]
  36. Rachid S., Ohlsen K., Witte W., Hacker J., Ziebuhr W. 2000; Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis . Antimicrob Agents Chemother 44:3357–3363 [View Article][PubMed]
     [Google Scholar]
  37. Sievers F., Wilm A., Dineen D., Gibson T. J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., other authors. 2011; Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 [View Article][PubMed]
     [Google Scholar]
  38. Thanweer F., Verma N. K. 2012; Identification of critical residues of the serotype modifying O-acetyltransferase of Shigella flexneri . BMC Biochem 13:13 [View Article][PubMed]
     [Google Scholar]
  39. Tormo M. Á., Martí M., Valle J., Manna A. C., Cheung A. L., Lasa I., Penadés J. R. 2005; SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol 187:2348–2356 [View Article][PubMed]
     [Google Scholar]
  40. Valle J., Toledo-Arana A., Berasain C., Ghigo J. M., Amorena B., Penadés J. R., Lasa I. 2003; SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus . Mol Microbiol 48:1075–1087 [View Article][PubMed]
     [Google Scholar]
  41. Van Arnam E. B., Lester H. A., Dougherty D. A. 2011; Dissecting the functions of conserved prolines within transmembrane helices of the D2 dopamine receptor. ACS Chem Biol 6:1063–1068 [View Article][PubMed]
     [Google Scholar]
  42. von Heijne G. 1992; Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487–494 [View Article][PubMed]
     [Google Scholar]
  43. Wang Q., Sun F.-J., Liu Y., Xiong L.-R., Xie L.-L., Xia P.-Y. 2010; Enhancement of biofilm formation by subinhibitory concentrations of macrolides in icaADBC-positive and -negative clinical isolates of Staphylococcus epidermidis . Antimicrob Agents Chemother 54:2707–2711 [View Article][PubMed]
     [Google Scholar]
  44. Weiss E. C., Zielinska A., Beenken K. E., Spencer H. J., Daily S. J., Smeltzer M. S. 2009; Impact of sarA on daptomycin susceptibility of Staphylococcus aureus biofilms in vivo . Antimicrob Agents Chemother 53:4096–4102 [View Article][PubMed]
     [Google Scholar]
  45. Woolfson D. N., Williams D. H. 1990; The influence of proline residues on α-helical structure. FEBS Lett 277:185–188 [View Article][PubMed]
     [Google Scholar]
  46. Wu D., Govindasamy L., Lian W., Gu Y., Kukar T., Agbandje-McKenna M., McKenna R. 2003; Structure of human carnitine acetyltransferase. Molecular basis for fatty acyl transfer. J Biol Chem 278:13159–13165 [View Article][PubMed]
     [Google Scholar]
  47. Yu N. Y., Wagner J. R., Laird M. R., Melli G., Rey S., Lo R., Dao P., Sahinalp S. C., Ester M., other authors. 2010; PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608–1615 [View Article][PubMed]
     [Google Scholar]
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Effects of erythromycin on the phenotypic and genotypic biofilm expression in two clinical Staphylococcus capitis subspecies and a functional analysis of Ica proteins in S. capitis
J. Med. Microbiol. 64, 591 (2015); https://doi.org/10.1099/jmm.0.000059
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