1887

Abstract

Subinhibitory concentrations (subMICs) of antibiotics may alter bacterial surface properties and change microbial physiology. This study aimed to investigate the effect of a subMIC (⅛ MIC) of penicillin (PEN) and erythromycin (ERY) on bacterial morphology, haemagglutinating activity, cell-surface hydrophobicity (CSH) and biofilm formation on glass and polystyrene surfaces, as well as the distribution of cell-surface acidic anionic residues of strains (HC01 strain; CDC-E8392 and 241 strains). All micro-organisms tested were susceptible to PEN and ERY. Growth in the presence of PEN induced bacterial filamentation, whereas subMIC of ERY caused cell-size reduction of strains 241 and CDC-E8392. Adherence to human erythrocytes was reduced after growth in the presence of ERY, while CSH was increased by a subMIC of both antibiotics in bacterial adherence to n-hexadecane assays. Conversely, antibiotic inhibition of biofilm formation was not observed. All strains enhanced biofilm formation on glass after treatment with ERY, while only strain 241 increased glass adherence after cultivation in the presence of PEN. Biofilm production on polystyrene surfaces was improved by ⅛ MIC of ERY. After growth in the presence of both antimicrobial agents, strains 241 and CDC-E8392 exhibited anionic surface charges with focal distribution. In conclusion, subMICs of PEN and ERY modified bacterial surface properties and enhanced not only biofilm formation but also cell-surface hydrophobicity. Antibiotic-induced biofilm formation may contribute to the inconsistent success of antimicrobial therapy for infections.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.052373-0
2013-05-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/5/754.html?itemId=/content/journal/jmm/10.1099/jmm.0.052373-0&mimeType=html&fmt=ahah

References

  1. Balagué C. , Fernández L. , Pérez J. , Grau R. . ( 2003; ). Effect of ciprofloxacin on adhesive properties of non-P mannose-resistant uropathogenic Escherichia coli isolates. . J Antimicrob Chemother 51:, 401–404. [CrossRef] [PubMed]
    [Google Scholar]
  2. Behrens S. H. , Grier D. G. . ( 2001; ). Pair interaction of charged colloidal spheres near a charged wall. . Phys Rev E Stat Nonlin Soft Matter Phys 64:, 050401. [CrossRef] [PubMed]
    [Google Scholar]
  3. Belmares J. , Detterline S. , Pak J. B. , Parada J. P. . ( 2007; ). Corynebacterium endocarditis species-specific risk factors and outcomes. . BMC Infect Dis 7:, 4. [CrossRef] [PubMed]
    [Google Scholar]
  4. Braga P. C. , Sasso M. D. , Sala M. T. . ( 2000; ). Sub-MIC concentrations of cefodizime interfere with various factors affecting bacterial virulence. . J Antimicrob Chemother 45:, 15–25. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chen K. , Sun G. W. , Chua K. L. , Gan Y. H. . ( 2005; ). Modified virulence of antibiotic-induced Burkholderia pseudomallei filaments. . Antimicrob Agents Chemother 49:, 1002–1009. [CrossRef] [PubMed]
    [Google Scholar]
  6. CLSI (2012). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; 9th edn, Approved Guideline M07-A9. Wayne, PA: Clinical and Laboratory Standards Institute.
  7. Colombo A. V. , Hirata R. Jr , de Souza C. M. , Monteiro-Leal L. H. , Previato J. O. , Formiga L. C. D. , Andrade A. F. B. , Mattos-Guaraldi A. L. . ( 2001; ). Corynebacterium diphtheriae surface proteins as adhesins to human erythrocytes. . FEMS Microbiol Lett 197:, 235–239. [CrossRef] [PubMed]
    [Google Scholar]
  8. 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]
  9. Davies J. , Spiegelman G. B. , Yim G. . ( 2006; ). The world of subinhibitory antibiotic concentrations. . Curr Opin Microbiol 9:, 445–453. [CrossRef] [PubMed]
    [Google Scholar]
  10. de Mattos-Guaraldi A. L. , Formiga L. C. D. . ( 1998; ). Bacteriological properties of a sucrose-fermenting Corynebacterium diphtheriae strain isolated from a case of endocarditis. . Curr Microbiol 37:, 156–158. [CrossRef] [PubMed]
    [Google Scholar]
  11. Di Bonaventura G. , Piccolomini R. , Paludi D. , D’Orio V. , Vergara A. , Conter M. , Ianieri A. . ( 2008; ). Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. . J Appl Microbiol 104:, 1552–1561. [CrossRef] [PubMed]
    [Google Scholar]
  12. Fonseca A. P. , Sousa J. C. . ( 2007; ). Effect of antibiotic-induced morphological changes on surface properties, motility and adhesion of nosocomial Pseudomonas aeruginosa strains under different physiological states. . J Appl Microbiol 103:, 1828–1837. [CrossRef] [PubMed]
    [Google Scholar]
  13. Fonseca A. P. , Extremina C. , Fonseca A. F. , Sousa J. C. . ( 2004; ). Effect of subinhibitory concentration of piperacillin/tazobactam on Pseudomonas aeruginosa . . J Med Microbiol 53:, 903–910. [CrossRef] [PubMed]
    [Google Scholar]
  14. Furneri P. M. , Garozzo A. , Musumarra M. P. , Scuderi A. C. , Russo A. , Bonfiglio G. . ( 2003; ). Effects on adhesiveness and hydrophobicity of sub-inhibitory concentrations of netilmicin. . Int J Antimicrob Agents 22:, 164–167. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gasic G. J. , Berwick L. , Sorrentino M. . ( 1968; ). Positive and negative colloidal iron as cell surface electron stains. . Lab Invest 18:, 63–71.[PubMed]
    [Google Scholar]
  16. Gomes D. L. , Martins C. A. , Faria L. M. , Santos L. S. , Santos C. S. , Sabbadini P. S. , Souza M. C. , Alves G. B. , Rosa A. C. et al. ( 2009; ). Corynebacterium diphtheriae as an emerging pathogen in nephrostomy catheter-related infection: evaluation of traits associated with bacterial virulence. . J Med Microbiol 58:, 1419–1427. [CrossRef] [PubMed]
    [Google Scholar]
  17. Grandière-Pérez L. , Jacqueline C. , Lemabecque V. , Patey O. , Potel G. , Caillon J. . ( 2005; ). Eagle effect in Corynebacterium diphtheriae . . J Infect Dis 191:, 2118–2120. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hirata R. Jr , Napoleão F. , Monteiro-Leal L. H. , Andrade A. F. B. , Nagao P. E. , Formiga L. C. D. , Fonseca L. S. , Mattos-Guaraldi A. L. . ( 2002; ). Intracellular viability of toxigenic Corynebacterium diphtheriae strains in HEp-2 cells. . FEMS Microbiol Lett 215:, 115–119. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hirata R. Jr , Souza S. M. , Rocha-de-Souza C. M. , Andrade A. F. , Monteiro-Leal L. H. , Formiga L. C. , Mattos-Guaraldi A. L. . ( 2004; ). Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. . Microb Pathog 36:, 125–130. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hirata R. Jr , Pereira G. A. , Filardy A. A. , Gomes D. L. R. , Damasco P. V. , Rosa A. C. P. , Nagao P. E. , Pimenta F. P. , Mattos-Guaraldi A. L. . ( 2008; ). Potential pathogenic role of aggregative-adhering Corynebacterium diphtheriae of different clonal groups in endocarditis. . Braz J Med Biol Res 41:, 986–991. [CrossRef] [PubMed]
    [Google Scholar]
  21. Hladka O. A. , Motyka O. I. . ( 1998; ). [The effect of antibiotics on the adhesion of Corynebacterium diphtheriae to buccal epithelial cells]. . Mikrobiol Z 60:, 60–64 (in Ukrainian).[PubMed]
    [Google Scholar]
  22. Hoffman L. R. , D’Argenio D. A. , MacCoss M. J. , Zhang Z. , Jones R. A. , Miller S. I. . ( 2005; ). Aminoglycoside antibiotics induce bacterial biofilm formation. . Nature 436:, 1171–1175. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kaplan J. B. . ( 2011; ). Antibiotic-induced biofilm formation. . Int J Artif Organs 34:, 737–751. [CrossRef] [PubMed]
    [Google Scholar]
  24. Kneen R. , Pham N. G. , Solomon T. , Tran T. M. , Nguyen T. T. , Tran B. L. , Wain J. , Day N. P. , Tran T. H. et al. ( 1998; ). Penicillin vs. erythromycin in the treatment of diphtheria. . Clin Infect Dis 27:, 845–850. [CrossRef] [PubMed]
    [Google Scholar]
  25. Kwaszewska A. K. , Brewczyńska A. , Szewczyk E. M. . ( 2006; ). Hydrophobicity and biofilm formation of lipophilic skin corynebacteria. . Pol J Microbiol 55:, 189–193.[PubMed] [CrossRef]
    [Google Scholar]
  26. Linares J. F. , Gustafsson I. , Baquero F. , Martinez J. L. . ( 2006; ). Antibiotics as intermicrobial signaling agents instead of weapons. . Proc Natl Acad Sci U S A 103:, 19484–19489. [CrossRef] [PubMed]
    [Google Scholar]
  27. Mattos-Guaraldi A. L. , Formiga L. C. D. . ( 1991; ). Relationship of biotype and source to the hemagglutination and adhesive properties of C. diphtheriae . . Braz J Med Biol Res 24:, 399–406.[PubMed]
    [Google Scholar]
  28. Mattos-Guaraldi A. L. , Formiga L. C. , Andrade A. F. . ( 1999; ). Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. . Curr Microbiol 38:, 37–42. [CrossRef] [PubMed]
    [Google Scholar]
  29. Menon T. , Senthilkumar S. , Pachaiyappan P. . ( 2010; ). Native valve endocarditis caused by a non-toxigenic strain of Corynebacterium diphtheriae . . Indian J Pathol Microbiol 53:, 899–900. [CrossRef] [PubMed]
    [Google Scholar]
  30. Mishra B. , Dignan R. J. , Hughes C. F. , Hendel N. . ( 2005; ). Corynebacterium diphtheriae endocarditis – surgery for some but not all!. Asian Cardiovasc Thorac Ann 13:, 119–126.[PubMed] [CrossRef]
    [Google Scholar]
  31. Morlot C. , Zapun A. , Dideberg O. , Vernet T. . ( 2003; ). Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. . Mol Microbiol 50:, 845–855. [CrossRef] [PubMed]
    [Google Scholar]
  32. Muttaiyah S. , Best E. J. , Freeman J. T. , Taylor S. L. , Morris A. J. , Roberts S. A. . ( 2011; ). Corynebacterium diphtheriae endocarditis: a case series and review of the treatment approach. . Int J Infect Dis 15:, e584–e588. [CrossRef] [PubMed]
    [Google Scholar]
  33. Nicolson G. L. . ( 1973; ). Anionic sites of human erythrocyte membranes. I. Effects of trypsin, phospholipase C, and pH on the topography of bound positively charged colloidal particles. . J Cell Biol 57:, 373–387. [CrossRef] [PubMed]
    [Google Scholar]
  34. O’Toole G. , Kaplan H. B. , Kolter R. . ( 2000; ). Biofilm formation as microbial development. . Annu Rev Microbiol 54:, 49–79. [CrossRef] [PubMed]
    [Google Scholar]
  35. Pereira G. A. , Pimenta F. P. , Santos F. R. , Damasco P. V. , Hirata Júnior R. , Mattos-Guaraldi A. L. . ( 2008; ). Antimicrobial resistance among Brazilian Corynebacterium diphtheriae strains. . Mem Inst Oswaldo Cruz 103:, 507–510. [CrossRef] [PubMed]
    [Google Scholar]
  36. Pérez-Núñez D. , Briandet R. , David B. , Gautier C. , Renault P. , Hallet B. , Hols P. , Carballido-López R. , Guédon E. . ( 2011; ). A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci. . Mol Microbiol 79:, 759–771. [CrossRef] [PubMed]
    [Google Scholar]
  37. Pimenta F. P. , Damasco P. V. , Cerbino Neto J. , Lopes G. S. , Hirata R. Jr , Milagres L. G. , Mattos-Guaraldi A. L. . ( 2006; ). Diphtheria-neutralizing antibody levels in healthy adults from Rio de Janeiro, Brazil. . Mem Inst Oswaldo Cruz 101:, 459–462. [CrossRef] [PubMed]
    [Google Scholar]
  38. Pompilio A. , Piccolomini R. , Picciani C. , D’Antonio D. , Savini V. , Di Bonaventura G. . ( 2008; ). Factors associated with adherence to and biofilm formation on polystyrene by Stenotrophomonas maltophilia: the role of cell surface hydrophobicity and motility. . FEMS Microbiol Lett 287:, 41–47. [CrossRef] [PubMed]
    [Google Scholar]
  39. Pompilio A. , Catavitello C. , Picciani C. , Confalone P. , Piccolomini R. , Savini V. , Fiscarelli E. , D’Antonio D. , Di Bonaventura G. . ( 2010; ). Subinhibitory concentrations of moxifloxacin decrease adhesion and biofilm formation of Stenotrophomonas maltophilia from cystic fibrosis. . J Med Microbiol 59:, 76–81. [CrossRef] [PubMed]
    [Google Scholar]
  40. Sabbadini P. S. , Assis M. C. , Trost E. , Gomes D. L. , Moreira L. O. , Dos Santos C. S. , Pereira G. A. , Nagao P. E. , Azevedo V. A. et al. ( 2012; ). Corynebacterium diphtheriae 67-72p hemagglutinin, characterized as the protein DIP0733, contributes to invasion and induction of apoptosis in HEp-2 cells. . Microb Pathog 52:, 165–176. [CrossRef] [PubMed]
    [Google Scholar]
  41. Stepanovic S. , Vukovic D. , Dakic I. , Savic B. , Svabic-Vlahovic M. . ( 2000; ). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. . J Microbiol Methods 40:, 175–179. [CrossRef] [PubMed]
    [Google Scholar]
  42. Subrt N. , Mesak L. R. , Davies J. . ( 2011; ). Modulation of virulence gene expression by cell wall active antibiotics in Staphylococcus aureus . . J Antimicrob Chemother 66:, 979–984. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sutton B. J. , Parsons A. C. , Palavecino E. L. . ( 2011; ). Filamentous bacteria masquerading as fungi: a diagnostic pitfall in direct smear interpretation with report of two cases. . J Clin Pathol 64:, 927–929. [CrossRef] [PubMed]
    [Google Scholar]
  44. Takahashi H. , Suda T. , Tanaka Y. , Kimura B. . ( 2010; ). Cellular hydrophobicity of Listeria monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl chloride. . Lett Appl Microbiol 50:, 618–625. [CrossRef] [PubMed]
    [Google Scholar]
  45. Tateda K. , Ishii Y. , Matsumoto T. , Kobayashi T. , Miyazaki S. , Yamaguchi K. . ( 2000; ). Potential of macrolide antibiotics to inhibit protein synthesis of Pseudomonas aeruginosa: suppression of virulence factors and stress response. . J Infect Chemother 6:, 1–7. [CrossRef] [PubMed]
    [Google Scholar]
  46. Viguetti S. Z. , Pacheco L. G. , Santos L. S. , Soares S. C. , Bolt F. , Baldwin A. , Dowson C. G. , Rosso M. L. et al. ( 2011; ). Multilocus sequence types of invasive Corynebacterium diphtheriae isolated in the Rio de Janeiro urban area, Brazil. . Epidemiol Infect 140:, 617–620.[PubMed] [CrossRef]
    [Google Scholar]
  47. von Hunolstein C. , Scopetti F. , Efstratiou A. , Engler K. . ( 2002; ). Penicillin tolerance amongst non-toxigenic Corynebacterium diphtheriae isolated from cases of pharyngitis. . J Antimicrob Chemother 50:, 125–128. [CrossRef] [PubMed]
    [Google Scholar]
  48. 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. [CrossRef] [PubMed]
    [Google Scholar]
  49. Wojnicz D. , Jankowski S. . ( 2007; ). Effects of subinhibitory concentrations of amikacin and ciprofloxacin on the hydrophobicity and adherence to epithelial cells of uropathogenic Escherichia coli strains. . Int J Antimicrob Agents 29:, 700–704. [CrossRef] [PubMed]
    [Google Scholar]
  50. Zapun A. , Vernet T. , Pinho M. G. . ( 2008; ). The different shapes of cocci. . FEMS Microbiol Rev 32:, 345–360. [CrossRef] [PubMed]
    [Google Scholar]
  51. Zasada A. A. , Zaleska M. , Podlasin R. B. , Seferynka I. . ( 2005; ). The first case of septicemia due to nontoxigenic Corynebacterium diphtheriae in Poland: case report. . Ann Clin Microbiol Antimicrob 4:, 1. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.052373-0
Loading
/content/journal/jmm/10.1099/jmm.0.052373-0
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