Biofilm induced tolerance towards antimicrobial peptides.

Anders Folkesson, Janus A J Haagensen, Claudia Zampaloni, Claus Sternberg, Søren Molin
Author Information
  1. Anders Folkesson: Infection Microbiology Group, BioCentrum-DTU, Technical University of Denmark, Lyngby, Denmark. anf@bio.dtu.dk

Abstract

Increased tolerance to antimicrobial agents is thought to be an important feature of microbes growing in biofilms. We address the question of how biofilm organization affects antibiotic susceptibility. We established Escherichia coli biofilms with differential structural organization due to the presence of IncF plasmids expressing altered forms of the transfer pili in two different biofilm model systems. The mature biofilms were subsequently treated with two antibiotics with different molecular targets, the peptide antibiotic colistin and the fluoroquinolone ciprofloxacin. The dynamics of microbial killing were monitored by viable count determination, and confocal laser microscopy. Strains forming structurally organized biofilms show an increased bacterial survival when challenged with colistin, compared to strains forming unstructured biofilms. The increased survival is due to genetically regulated tolerant subpopulation formation and not caused by a general biofilm property. No significant difference in survival was detected when the strains were challenged with ciprofloxacin. Our data show that biofilm formation confers increased colistin tolerance to cells within the biofilm structure, but the protection is conditional being dependent on the structural organization of the biofilm, and the induction of specific tolerance mechanisms.

References

  1. Respir Med. 2000 Jul;94(7):632-40 [PMID: 10926333]
  2. Antimicrob Agents Chemother. 2001 Apr;45(4):999-1007 [PMID: 11257008]
  3. J Mol Biol. 1983 Oct 15;170(1):61-91 [PMID: 6313938]
  4. Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5 [PMID: 10829079]
  5. J Bacteriol. 1993 Mar;175(5):1384-91 [PMID: 8095257]
  6. Nat Rev Microbiol. 2005 Jan;3(1):36-46 [PMID: 15608698]
  7. J Bacteriol. 2006 May;188(10):3572-81 [PMID: 16672611]
  8. J Bacteriol. 2003 May;185(10):3111-7 [PMID: 12730171]
  9. Appl Environ Microbiol. 1998 Nov;64(11):4115-27 [PMID: 9797255]
  10. J Antimicrob Chemother. 1998 Aug;42(2):153-60 [PMID: 9738832]
  11. Annu Rev Microbiol. 1995;49:711-45 [PMID: 8561477]
  12. Microbiol Mol Biol Rev. 1997 Sep;61(3):377-92 [PMID: 9293187]
  13. Biosci Biotechnol Biochem. 2004 Aug;68(8):1758-67 [PMID: 15322361]
  14. Int J Antimicrob Agents. 2005 Jan;25(1):11-25 [PMID: 15620821]
  15. J Bacteriol. 1951 Sep;62(3):293-300 [PMID: 14888646]
  16. J Biol Chem. 2001 Nov 16;276(46):43132-44 [PMID: 11535605]
  17. Nature. 2003 Nov 20;426(6964):306-10 [PMID: 14628055]
  18. Antimicrob Agents Chemother. 1992 Jun;36(6):1208-14 [PMID: 1416820]
  19. J Bacteriol. 2007 Jan;189(1):28-37 [PMID: 17041046]
  20. Biol Proced Online. 2003;5:189-196 [PMID: 14615815]
  21. Antimicrob Agents Chemother. 1995 May;39(5):1038-44 [PMID: 7625785]
  22. Microbiology (Reading). 2000 Mar;146 ( Pt 3):547-549 [PMID: 10746758]
  23. APMIS. 1996 Apr;104(4):280-4 [PMID: 8645467]
  24. J Bacteriol. 1998 May;180(9):2442-9 [PMID: 9573197]
  25. Microbiology (Reading). 2000 Oct;146 ( Pt 10):2395-2407 [PMID: 11021916]
  26. J Antimicrob Chemother. 1999 Jul;44(1):43-55 [PMID: 10459809]
  27. J Clin Microbiol. 2005 Oct;43(10):5085-90 [PMID: 16207967]
  28. J Bacteriol. 1993 Mar;175(5):1375-83 [PMID: 8444800]
  29. Microbes Infect. 2003 Nov;5(13):1213-9 [PMID: 14623017]
  30. Appl Environ Microbiol. 1998 Jun;64(6):2247-55 [PMID: 9603843]
  31. Nature. 2001 Jul 26;412(6845):442-5 [PMID: 11473319]
  32. J Vet Med Sci. 2005 Oct;67(10):999-1003 [PMID: 16276055]
  33. FEBS Lett. 1981 Jun 29;129(1):145-9 [PMID: 6268456]
  34. Antimicrob Agents Chemother. 1989 Oct;33(10):1724-8 [PMID: 2556077]
  35. Drugs. 1999;58 Suppl 2:6-10 [PMID: 10553698]
  36. Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17162-7 [PMID: 15569938]
  37. J Bacteriol. 1979 Feb;137(2):1043-7 [PMID: 217864]
  38. Appl Environ Microbiol. 1998 Jun;64(6):2240-6 [PMID: 9603842]
  39. J Bacteriol. 1985 May;162(2):584-90 [PMID: 2859268]
  40. J Bacteriol. 1995 Jun;177(11):2957-64 [PMID: 7768788]
  41. Antimicrob Agents Chemother. 1989 Jun;33(6):813-6 [PMID: 2764528]
  42. Microbiology (Reading). 1997 Jul;143 ( Pt 7):2407-2413 [PMID: 9245822]
  43. J Bacteriol. 2001 Dec;183(23):6746-51 [PMID: 11698361]
  44. Annu Rev Biochem. 1977;46:723-63 [PMID: 197881]
  45. Adv Dent Res. 1997 Apr;11(1):160-7 [PMID: 9524452]
  46. Plasmid. 1991 Jul;26(1):40-54 [PMID: 1658835]
  47. Appl Environ Microbiol. 1999 Sep;65(9):4108-17 [PMID: 10473423]
  48. Antimicrob Agents Chemother. 1993 Sep;37(9):2000-2 [PMID: 7694545]
  49. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4772-6 [PMID: 337300]
  50. Plasmid. 1992 Jul;28(1):14-24 [PMID: 1387714]
  51. J Bacteriol. 2006 May;188(10):3582-8 [PMID: 16672612]
  52. Mol Microbiol. 1996 Oct;22(2):197-205 [PMID: 8930905]
  53. Curr Opin Biotechnol. 2003 Jun;14(3):255-61 [PMID: 12849777]
  54. Nature. 2002 Apr 18;416(6882):740-3 [PMID: 11961556]
  55. J Clin Microbiol. 1999 Jun;37(6):1771-6 [PMID: 10325322]
  56. Appl Environ Microbiol. 2002 Apr;68(4):2008-17 [PMID: 11916724]
  57. Pharmacol Rev. 2003 Mar;55(1):27-55 [PMID: 12615953]
  58. J Bacteriol. 2002 May;184(10):2767-79 [PMID: 11976307]
  59. Mol Microbiol. 2003 May;48(4):933-46 [PMID: 12753187]
  60. FEMS Microbiol Rev. 2000 Dec;24(5):661-71 [PMID: 11077157]
  61. Appl Environ Microbiol. 1998 Oct;64(10):4035-9 [PMID: 9758837]
  62. Infect Immun. 2006 Apr;74(4):2102-14 [PMID: 16552039]
  63. Antimicrob Agents Chemother. 1985 Apr;27(4):619-24 [PMID: 3923925]

MeSH Term

Antimicrobial Cationic Peptides
Biofilms
Ciprofloxacin
Colistin
Drug Resistance, Bacterial
Drug Resistance, Microbial
Drug Tolerance
Escherichia coli
Flow Cytometry
Fluoroquinolones
Microbial Sensitivity Tests
Microscopy, Confocal
Mutation
Plasmids

Chemicals

Antimicrobial Cationic Peptides
Fluoroquinolones
Ciprofloxacin
Colistin

Word Cloud

Created with Highcharts 10.0.0biofilmbiofilmstoleranceorganizationcolistinincreasedsurvivalantimicrobialantibioticstructuralduetwodifferentciprofloxacinformingshowchallengedstrainsformationIncreasedagentsthoughtimportantfeaturemicrobesgrowingaddressquestionaffectssusceptibilityestablishedEscherichiacolidifferentialpresenceIncFplasmidsexpressingalteredformstransferpilimodelsystemsmaturesubsequentlytreatedantibioticsmoleculartargetspeptidefluoroquinolonedynamicsmicrobialkillingmonitoredviablecountdeterminationconfocallasermicroscopyStrainsstructurallyorganizedbacterialcomparedunstructuredgeneticallyregulatedtolerantsubpopulationcausedgeneralpropertysignificantdifferencedetecteddataconferscellswithinstructureprotectionconditionaldependentinductionspecificmechanismsBiofilminducedtowardspeptides

Similar Articles

Cited By