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PMID: 17993517 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa.

Journal of bacteriology ·Vol. 190 ·No. 2 ·2008-01-00 ·Pages 662-71

Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP, Poole K

Abstract

Reducing iron (Fe) levels in a defined minimal medium reduced the growth yields of planktonic and biofilm Pseudomonas aeruginosa, though biofilm biomass was affected to the greatest extent and at FeCl3 concentrations where planktonic cell growth was not compromised. Highlighting this apparently greater need for Fe, biofilm growth yields were markedly reduced in a mutant unable to produce pyoverdine (and, so, deficient in pyoverdine-mediated Fe acquisition) at concentrations of FeCl3 that did not adversely affect biofilm yields of a pyoverdine-producing wild-type strain. Concomitant with the reduced biofilm yields at low Fe concentrations, P. aeruginosa showed enhanced twitching motility in Fe-deficient versus Fe-replete minimal media. A mutant deficient in low-Fe-stimulated twitching motility but normal as regards twitching motility on Fe-rich medium was isolated and shown to be disrupted in rhlI, whose product is responsible for synthesis of the N-butanoyl homoserine lactone (C4-HSL) quorum-sensing signal. In contrast to wild-type cells, which formed thin, flat, undeveloped biofilms in Fe-limited medium, the rhlI mutant formed substantially developed though not fully mature biofilms under Fe limitation. C4-HSL production increased markedly in Fe-limited versus Fe-rich P. aeruginosa cultures, and cell-free low-Fe culture supernatants restored the twitching motility of the rhlI mutant on Fe-limited minimal medium and stimulated the twitching motility of rhlI and wild-type P. aeruginosa on Fe-rich minimal medium. Still, addition of exogenous C4-HSL did not stimulate the twitching motility of either strain on Fe-replete medium, indicating that some Fe-regulated and RhlI/C4-HSL-dependent extracellular product(s) was responsible for the enhanced twitching motility (and reduced biofilm formation) seen in response to Fe limitation.

MeSH Terms
4-Butyrolactone/analogs & derivatives,biosynthesis Biofilms/growth & development Culture Media/chemistry Iron/metabolism Ligases/genetics Locomotion/genetics,physiology Mutagenesis, Insertional Oligopeptides/biosynthesis Pseudomonas aeruginosa/genetics,physiology Quorum Sensing/physiology Transcription Factors/genetics
Chemicals
Culture Media N-butyrylhomoserine lactone Oligopeptides Transcription Factors pyoverdin Iron Ligases RHLI protein, Pseudomonas aeruginosa 4-Butyrolactone
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Patriquin Glenn M
Queen's University, Department of Microbiology and Immunology, Rm. 737, Botterell Hall, Kingston, Ontario, Canada.
Banin Ehud
Gilmour Christie
Tuchman Rivka
Greenberg E Peter
Poole Keith
References (80)
80 references, click to expand
  1. Airway biofilms: implications for pathogenesis and therapy of respiratory tract infections.
    Treat Respir Med. 2005;4(4):241-53 PMID: 16086598
  2. A simple in vitro model for growth control of bacterial biofilms.
    J Appl Bacteriol. 1995 Jul;79(1):87-93 PMID: 11419484
  3. Antimicrobial resistance of Pseudomonas aeruginosa biofilms.
    Microbes Infect. 2003 Nov;5(13):1213-9 PMID: 14623017
  4. Bacterial biofilms within the clinical setting: what healthcare professionals should know.
    J Hosp Infect. 2006 Dec;64(4):313-25 PMID: 17046102
  5. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis.
    Dev Cell. 2002 Oct;3(4):593-603 PMID: 12408810
  6. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms.
    FEMS Microbiol Lett. 2006 Aug;261(1):1-11 PMID: 16842351
  7. Mutations in PA2491 (mexS) promote MexT-dependent mexEF-oprN expression and multidrug resistance in a clinical strain of Pseudomonas aeruginosa.
    J Bacteriol. 2005 Feb;187(4):1246-53 PMID: 15687188
  8. The physiology and collective recalcitrance of microbial biofilm communities.
    Adv Microb Physiol. 2002;46:202-56 PMID: 12073654
  9. Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions.
    Biotechniques. 2000 Nov;29(5):948-50, 952 PMID: 11084852
  10. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.
    Mol Microbiol. 1998 Oct;30(2):295-304 PMID: 9791175
  11. Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities?
    Cell Microbiol. 2006 Dec;8(12):1841-9 PMID: 17026480
  12. Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa: involvement of a probable extracytoplasmic-function sigma factor, FpvI.
    J Bacteriol. 2003 Feb;185(4):1261-5 PMID: 12562796
  13. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family.
    J Bacteriol. 1995 Dec;177(24):7155-63 PMID: 8522523
  14. Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density.
    Microbiology (Reading). 2005 Apr;151(Pt 4):1127-1138 PMID: 15817780
  15. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis.
    Mol Microbiol. 1998 May;28(3):449-61 PMID: 9632250
  16. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients.
    Curr Opin Pediatr. 2007 Feb;19(1):83-8 PMID: 17224667
  17. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa.
    Int J Med Microbiol. 2006 Apr;296(2-3):73-81 PMID: 16476569
  18. Spatial patterns of alkaline phosphatase expression within bacterial colonies and biofilms in response to phosphate starvation.
    Appl Environ Microbiol. 1998 Apr;64(4):1526-31 PMID: 9546188
  19. Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates.
    Antimicrob Agents Chemother. 2003 Oct;47(10):3202-7 PMID: 14506031
  20. Bacterial evasion of antimicrobial peptides by biofilm formation.
    Curr Top Microbiol Immunol. 2006;306:251-8 PMID: 16909925
  21. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation.
    J Bacteriol. 2001 Mar;183(6):1990-6 PMID: 11222597
  22. Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation.
    Biometals. 2004 Jun;17(3):267-70 PMID: 15222476
  23. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways.
    J Bacteriol. 2006 Dec;188(24):8601-6 PMID: 17028277
  24. Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes.
    Genome Res. 2005 Apr;15(4):583-9 PMID: 15805499
  25. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  26. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6424-8 PMID: 7604006
  27. Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems.
    J Bacteriol. 2007 Jul;189(13):4827-36 PMID: 17449617
  28. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa.
    Chem Biol. 2005 Jul;12(7):789-96 PMID: 16039526
  29. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns.
    Appl Environ Microbiol. 2001 Apr;67(4):1865-73 PMID: 11282644
  30. FpvA-mediated ferric pyoverdine uptake in Pseudomonas aeruginosa: identification of aromatic residues in FpvA implicated in ferric pyoverdine binding and transport.
    J Bacteriol. 2005 Dec;187(24):8511-5 PMID: 16321958
  31. Genetic systems in Haemophilus influenzae.
    Methods Enzymol. 1991;204:321-42 PMID: 1943781
  32. Type IV pili and twitching motility.
    Annu Rev Microbiol. 2002;56:289-314 PMID: 12142488
  33. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids.
    Microbiology (Reading). 2003 Aug;149(Pt 8):2005-2013 PMID: 12904540
  34. Bacterial biofilms: from the natural environment to infectious diseases.
    Nat Rev Microbiol. 2004 Feb;2(2):95-108 PMID: 15040259
  35. Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis.
    Curr Opin Pharmacol. 2007 Jun;7(3):244-51 PMID: 17418640
  36. The involvement of cell-to-cell signals in the development of a bacterial biofilm.
    Science. 1998 Apr 10;280(5361):295-8 PMID: 9535661
  37. Analysis of random and site-directed mutations in rhII, a Pseudomonas aeruginosa gene encoding an acylhomoserine lactone synthase.
    Mol Microbiol. 1997 Oct;26(2):301-10 PMID: 9383155
  38. Comprehensive transposon mutant library of Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14339-44 PMID: 14617778
  39. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms.
    Appl Environ Microbiol. 2002 Sep;68(9):4457-64 PMID: 12200300
  40. Diversity of biofilms produced by quorum-sensing-deficient clinical isolates of Pseudomonas aeruginosa.
    J Med Microbiol. 2007 Jun;56(Pt 6):738-748 PMID: 17510257
  41. Both lactoferrin and iron influence aggregation and biofilm formation in Streptococcus mutans.
    Biometals. 2004 Jun;17(3):271-8 PMID: 15222477
  42. The role of biofilms in airway disease.
    Semin Respir Crit Care Med. 2003 Dec;24(6):663-70 PMID: 16088582
  43. Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium.
    Microbiology (Reading). 2002 Aug;148(Pt 8):2371-2381 PMID: 12177331
  44. A re-examination of twitching motility in Pseudomonas aeruginosa.
    Microbiology (Reading). 1999 Oct;145 ( Pt 10):2863-73 PMID: 10537208
  45. MexAB-OprM hyperexpression in NalC-type multidrug-resistant Pseudomonas aeruginosa: identification and characterization of the nalC gene encoding a repressor of PA3720-PA3719.
    Mol Microbiol. 2004 Sep;53(5):1423-36 PMID: 15387820
  46. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1.
    Mol Microbiol. 1995 Jul;17(2):333-43 PMID: 7494482
  47. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR.
    J Bacteriol. 1988 Jun;170(6):2575-83 PMID: 2836362
  48. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation.
    J Microbiol Methods. 2006 Mar;64(3):391-7 PMID: 15987659
  49. Multicellular organization in a degradative biofilm community.
    Appl Environ Microbiol. 1994 Feb;60(2):434-46 PMID: 16349173
  50. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional.
    Mol Microbiol. 2006 Dec;62(5):1264-77 PMID: 17059568
  51. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa.
    J Bacteriol. 2007 Jul;189(14):5383-6 PMID: 17496081
  52. Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains.
    Plasmid. 2000 Jan;43(1):59-72 PMID: 10610820
  53. Iron and Pseudomonas aeruginosa biofilm formation.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11076-81 PMID: 16043697
  54. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound.
    Microbiology (Reading). 2002 Jan;148(Pt 1):87-102 PMID: 11782502
  55. Biofilms and antimicrobial resistance.
    Clin Orthop Relat Res. 2005 Aug;(437):41-7 PMID: 16056024
  56. Interaction of biofilm bacteria with antibiotics in a novel in vitro chemostat system.
    Antimicrob Agents Chemother. 1989 Oct;33(10):1824-6 PMID: 2511804
  57. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms.
    Nature. 2000 Oct 12;407(6805):762-4 PMID: 11048725
  58. The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity.
    Environ Microbiol. 2006 Aug;8(8):1318-29 PMID: 16872396
  59. The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication.
    Microbiology (Reading). 2005 Apr;151(Pt 4):1113-1125 PMID: 15817779
  60. Quorum sensing: the power of cooperation in the world of Pseudomonas.
    Environ Microbiol. 2005 Apr;7(4):459-71 PMID: 15816912
  61. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants.
    Gene. 1991 Jan 2;97(1):39-47 PMID: 1847347
  62. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms.
    J Clin Microbiol. 1999 Jun;37(6):1771-6 PMID: 10325322
  63. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression.
    Appl Environ Microbiol. 2002 Apr;68(4):2008-17 PMID: 11916724
  64. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms.
    Mol Microbiol. 2003 Oct;50(1):61-8 PMID: 14507363
  65. A component of innate immunity prevents bacterial biofilm development.
    Nature. 2002 May 30;417(6888):552-5 PMID: 12037568
  66. High efficiency transformation of Escherichia coli with plasmids.
    Gene. 1990 Nov 30;96(1):23-8 PMID: 2265755
  67. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility.
    J Bacteriol. 1999 Mar;181(5):1623-9 PMID: 10049396
  68. Pyoverdine-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein.
    FEMS Microbiol Lett. 1991 Feb;62(1):1-5 PMID: 1903349
  69. Assembly of the MexAB-OprM multidrug efflux system of Pseudomonas aeruginosa: identification and characterization of mutations in mexA compromising MexA multimerization and interaction with MexB.
    J Bacteriol. 2004 May;186(10):2973-83 PMID: 15126457
  70. Iron-responsive regulation of biofilm formation in staphylococcus aureus involves fur-dependent and fur-independent mechanisms.
    J Bacteriol. 2005 Dec;187(23):8211-5 PMID: 16291697
  71. Bacterial biofilms: an emerging link to disease pathogenesis.
    Annu Rev Microbiol. 2003;57:677-701 PMID: 14527295
  72. GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes.
    Mol Microbiol. 2002 Sep;45(5):1277-87 PMID: 12207696
  73. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa.
    Microbiology (Reading). 2007 May;153(Pt 5):1318-1328 PMID: 17464046
  74. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants.
    Mol Microbiol. 2003 Jun;48(6):1511-24 PMID: 12791135
  75. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa.
    J Bacteriol. 2002 Jul;184(13):3598-604 PMID: 12057954
  76. Basic features of biofilms--why are they difficult therapeutic targets?
    Ann R Australas Coll Dent Surg. 2004 Oct;17:30-4 PMID: 16479852
  77. Gene expression in Pseudomonas aeruginosa biofilms.
    Nature. 2001 Oct 25;413(6858):860-4 PMID: 11677611
  78. Functional cloning and characterization of a multidrug efflux pump, mexHI-opmD, from a Pseudomonas aeruginosa mutant.
    Antimicrob Agents Chemother. 2003 Sep;47(9):2990-2 PMID: 12937010
  79. Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling.
    Infect Immun. 2007 Aug;75(8):3715-21 PMID: 17562773
  80. Recurring and antimicrobial-resistant infections:considering the potential role of biofilms in clinical practice.
    Ostomy Wound Manage. 2007 Apr;53(4):46-8, 50, 52 passim PMID: 17449916
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
1098-5530
Published
2008-01-00
Epub
2007-00-09
Pages
662-71
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC2223716
Subset
IM
Grants
PHS HHS · A130040 · United States
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