1887

Abstract

, a versatile bacterium present in terrestrial and aquatic environments and a relevant opportunistic human pathogen, is largely known for the production of robust biofilms. The unique properties of these structures complicate biofilm eradication, because they make the biofilms very resistant to diverse antibacterial agents. Biofilm development and establishment is a complex process regulated by multiple regulatory genetic systems, among them is quorum sensing (QS), a mechanism employed by bacteria to regulate gene transcription in response to population density. In addition, environmental factors such as UVA radiation (400–315 nm) have been linked to biofilm formation. In this work, we further investigate the mechanism underlying the induction of biofilm formation by UVA, analysing the role of QS in this phenomenon. We demonstrate that UVA induces key genes of the Las and Rhl QS systems at the transcriptional level. We also report that and genes, which are essential for biofilm formation and whose transcription depends in part on QS, are significantly induced under UVA exposure. Finally, the results demonstrate that in a strain (impaired for ppGpp production), the UVA treatment does not induce biofilm formation or QS genes, suggesting that the increase of biofilm formation due to exposure to UVA in could rely on a ppGpp-dependent QS induction.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000932
2020-06-04
2020-09-20
Loading full text...

Full text loading...

References

  1. Høiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 2010; 11:1663–1674
    [Google Scholar]
  2. Willcox MD, Harmis N, Cowell W, Holden T. Bacterial interactions with contact lenses; effects of lens material, lens wear and microbial physiology. Biomaterials 2001; 22:3235–3247
    [Google Scholar]
  3. Rajasekar A, Anandkumar B, Maruthamuthu S, Ting YP, Rahman P. Characterization of corrosive bacterial consortia isolated from petroleum product-transporting pipelines. Appl Microbiol Biotechnol 2010; 85:1175–1188
    [Google Scholar]
  4. Elasri MO, Miller RV. Study of the response of a biofilm bacterial community to UV radiation. Appl Environ Microbiol 1999; 65:2025–2031
    [Google Scholar]
  5. Hassett DJ, Ma J-F, Elkins JG, McDermott TR, Ochsner UA et al. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 1999; 34:1082–1093 [CrossRef][PubMed]
    [Google Scholar]
  6. Mah T-FC, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001; 9:34–39 [CrossRef][PubMed]
    [Google Scholar]
  7. Pezzoni M, Pizarro RA, Costa CS. Protective role of extracellular catalase (KatA) against UVA radiation in Pseudomonas aeruginosa biofilms. J Photochem Photobiol B 2014; 131:53–64 [CrossRef][PubMed]
    [Google Scholar]
  8. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000; 54:49–79 [CrossRef][PubMed]
    [Google Scholar]
  9. Sauer K, Cullen MC, Rickard AH, Zeef LAH, Davies DG et al. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 2004; 186:7312–7326
    [Google Scholar]
  10. Fazli M, Almblad H, Rybtke ML, Givskov M, Eberl L et al. Regulation of biofilm formation in Pseudomonas and Burkholderia species. Environ Microbiol 2014; 16:1961–1968
    [Google Scholar]
  11. Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 2009; 7:263–273
    [Google Scholar]
  12. Gottesman S, Storz G. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 2011; 3:a003798 [CrossRef][PubMed]
    [Google Scholar]
  13. Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 2009; 72:612–632 [CrossRef][PubMed]
    [Google Scholar]
  14. Michaux C, Verneuil N, Hartke A, Giard J-C. Physiological roles of small RNA molecules. Microbiology 2014; 160:1007–1019 [CrossRef][PubMed]
    [Google Scholar]
  15. Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 2001; 35:439–468 [CrossRef][PubMed]
    [Google Scholar]
  16. Solano C, Echeverz M, Lasa I. Biofilm dispersion and quorum sensing. Curr Opin Microbiol 2014; 18:96104 [CrossRef][PubMed]
    [Google Scholar]
  17. Pearson JP, Passador L, Iglewski BH, Greenberg EP. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa . Proc Natl Acad Sci USA 1995; 92:1490–1494 [CrossRef][PubMed]
    [Google Scholar]
  18. Passador L, Cook JM, Gambello MJ, Rust L, Iglewski BH. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 1993; 260:1127–1130
    [Google Scholar]
  19. Sifri CD. Quorum sensing: bacteria talk sense. Clin Infect Dis 2008; 47:1070–1076
    [Google Scholar]
  20. Verbeke F, De Craemer S, Debunne N, Janssens Y, Wynendaele E et al. Peptides as quorum sensing molecules: measurement techniques and obtained levels in vitro and in vivo. Front Neurosci 2017; 12:11–18
    [Google Scholar]
  21. Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 1999; 96:11229–11234 [CrossRef][PubMed]
    [Google Scholar]
  22. McKnight SL, Iglewski BH, Pesci EC. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 2000; 182:2702–2708
    [Google Scholar]
  23. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW et al. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998; 280:295–298
    [Google Scholar]
  24. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB et al. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 2002; 148:87–102 [CrossRef][PubMed]
    [Google Scholar]
  25. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS et al. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 2006; 59:1114–1128 [CrossRef][PubMed]
    [Google Scholar]
  26. Pamp SJ, Tolker-Nielsen T. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa . J Bacteriol 2007; 189:2531–2539 [CrossRef][PubMed]
    [Google Scholar]
  27. Gilbert KB, Kim TH, Gupta R, Greenberg E, Schuster M. Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol Microbiol 2009; 73:1072–1085
    [Google Scholar]
  28. Sakuragi Y, Kolter R. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa . J Bacteriol 2007; 189:5383–5386 [CrossRef][PubMed]
    [Google Scholar]
  29. Di Bonaventura G, Stepanović S, Picciani C, Pompilio A, Piccolomini R. Effect of environmental factors on biofilm formation by clinical Stenotrophomonas maltophilia isolates. Folia Microbiol 2007; 52:86–90
    [Google Scholar]
  30. Garrett TR, Bhakoo M, Zhang Z. Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 2008; 18:1049–1056 [CrossRef]
    [Google Scholar]
  31. Ben Said M, Khefacha S, Maalej L, Dalu I, Hassen A. Effect of ultraviolet, electromagnetic radiation subtype C (UV-C) dose on biofilm formation by Pseudomonas aeruginoisa . Afr J Microbiol Res 2011; 5:4353–4358
    [Google Scholar]
  32. Gambino M, Cappitelli F. Mini-review: biofilm responses to oxidative stress. Biofouling 2016; 32:167–178 [CrossRef][PubMed]
    [Google Scholar]
  33. Pezzoni M, Pizarro RA, Costa CS. Exposure to low doses of UVA increases biofilm formation in Pseudomonas aeruginosa . Biofouling 2018; 34:673–684 [CrossRef][PubMed]
    [Google Scholar]
  34. Webb RB. Lethal and mutagenic effects of near-ultraviolet radiation. Photochem Photobiol Rev 1977; 2:169–261
    [Google Scholar]
  35. Fernández RO, Pizarro RA. Lethal effect induced in Pseudomonas aeruginosa exposed to ultraviolet-A radiation. Photochem Photobiol 1996; 64:334–339 [CrossRef][PubMed]
    [Google Scholar]
  36. Fernández RO, Pizarro RA. Pseudomonas aeruginosa UV-A-induced lethal effect: influence of salts, nutritional stress and pyocyanine. J Photochem Photobiol B 1999; 50:59–65 [CrossRef][PubMed]
    [Google Scholar]
  37. Baümler W, Regensburger J, Knak A, Felgenträger A, Maisch T. UVA and endogenous photosensitizers the detection of singlet oxygen by its luminescence. Photochem Photobiol 2012; 11:107–117
    [Google Scholar]
  38. Pezzoni M, Meichtry M, Pizarro RA, Costa CS. Role of the Pseudomonas quinolone signal (PQS) in sensitising Pseudomonas aeruginosa to UVA radiation. J Photochem Photobiol B 2015; 142:129–140 [CrossRef]
    [Google Scholar]
  39. Gamage J, Zhang Z. Applications of photocatalytic disinfection. Int J Photoenergy 2010; 2010:764870 [CrossRef]
    [Google Scholar]
  40. McGuigan KG, Conroy RM, Mosler H-J, du Preez M, Ubomba-Jaswa E et al. Solar water disinfection (SODIS): a review from bench-top to roof-top. J Hazard Mater 2012; 235-236:29–46 [CrossRef][PubMed]
    [Google Scholar]
  41. Jagger J. Near UV radiation effects on microorganisms. Photochem Photobiol 1981; 34:761–768
    [Google Scholar]
  42. Day RS, Muel B. Ultraviolet inactivation of the ability of Escherichia coli to support the growth of phage T7: an action spectrum. Photochem Photobiol 1974; 20:98–102
    [Google Scholar]
  43. Berney M, Weilenmann H-U, Egli T. Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environ Microbiol 2006; 8:1635–1647 [CrossRef][PubMed]
    [Google Scholar]
  44. Soule T, Gao Q, Stout V, Garcia-Pichel F. The global response of Nostoc punctiforme ATCC 29133 to UVA stress, assessed in a temporal DNA microarray study. Photochem Photobiol 2013; 89:415–423 [CrossRef][PubMed]
    [Google Scholar]
  45. Sassoubre LM, Ramsey MM, Gilmore MS, Boehm AB. Transcriptional response of Enterococcus faecalis to sunlight. J Photochem Photobiol B 2014; 130:349–356 [CrossRef][PubMed]
    [Google Scholar]
  46. Pezzoni M, Tribelli PM, Pizarro RA, López NI, Costa CS. Exposure to low UVA doses increases KatA and KatB catalase activities, and confers cross-protection against subsequent oxidative injuries in Pseudomonas aeruginosa . Microbiology 2016; 162:855–864 [CrossRef][PubMed]
    [Google Scholar]
  47. Schuster M, Lostroh CP, Ogi T, Greenberg EP. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 2003; 185:2066–2079 [CrossRef][PubMed]
    [Google Scholar]
  48. Friedman L, Kolter R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 2004; 51:675–690 [CrossRef][PubMed]
    [Google Scholar]
  49. Hoerter JD, Arnold AA, Kuczynska DA, Shibuya A, Ward CS et al. Effects of sublethal UVA irradiation on activity levels of oxidative defense enzymes and protein oxidation in Escherichia coli . J Photochem Photobiol B 2005; 81:171–180 [CrossRef][PubMed]
    [Google Scholar]
  50. Chang W-S, van de Mortel M, Nielsen L, Nino de Guzman G, Li X et al. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 2007; 189:8290–8299 [CrossRef][PubMed]
    [Google Scholar]
  51. Tielen P, Rosenau F, Wilhelm S, Jaeger K-E, Flemming H-C et al. Extracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa . Microbiology 2010; 156:2239–2252 [CrossRef][PubMed]
    [Google Scholar]
  52. Messiaen AS, Nelis H, Coenye T. Investigating the role of matrix components in protection of Burkholderia cepacia complex biofilms against tobramycin. J Cyst Fibros 2014; 13:56–62
    [Google Scholar]
  53. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem 1956; 28:350–356 [CrossRef]
    [Google Scholar]
  54. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193:265–275[PubMed]
    [Google Scholar]
  55. Erickson DL, Lines JL, Pesci EC, Venturi V, Storey DG. Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster . Infect Immun 2004; 72:5638–5645 [CrossRef][PubMed]
    [Google Scholar]
  56. Costa CS, Pezzoni M, Fernández RO, Pizarro RA. Role of the quorum sensing mechanism in the response of Pseudomonas aeruginosa to lethal and sublethal UVA irradiation. Photochem Photobiol 2010; 86:1334–1342 [CrossRef][PubMed]
    [Google Scholar]
  57. Erickson DL, Endersby R, Kirkham A, Stuber K, Vollman DD et al. Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 2002; 70:1783–1790 [CrossRef][PubMed]
    [Google Scholar]
  58. Miller JH. Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1972
    [Google Scholar]
  59. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinform 2005; 6:62
    [Google Scholar]
  60. Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 2010; 59:253–268 [CrossRef][PubMed]
    [Google Scholar]
  61. Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M et al. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa . Microbiology 2007; 153:1318–1328 [CrossRef][PubMed]
    [Google Scholar]
  62. Wozniak DJ, Wyckoff TJO, Starkey M, Keyser R, Azadi P et al. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci USA 2003; 100:7907–7912 [CrossRef]
    [Google Scholar]
  63. Ryder C, Byrd M, Wozniak DJ. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 2007; 10:644–648
    [Google Scholar]
  64. Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 2005; 151:985–997 [CrossRef][PubMed]
    [Google Scholar]
  65. Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC et al. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 2012; 14:1913–1928 [CrossRef][PubMed]
    [Google Scholar]
  66. Van Delden C, Comte R, Bally M. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa . J Bacteriol 2001; 183:5376–5384 [CrossRef][PubMed]
    [Google Scholar]
  67. Schafhauser J, Lepine F, McKay G, Ahlgren HG, Khakimova M et al. The stringent response modulates 4-hydroxy-2-alkylquinoline biosynthesis and quorum-sensing hierarchy in Pseudomonas aeruginosa . J Bacteriol 2014; 196:1641–1650 [CrossRef][PubMed]
    [Google Scholar]
  68. Yan X, Zhao C, Budin-Verneuil A, Hartke A, Rincé A et al. The (p)ppGpp synthetase RelA contributes to stress adaptation and virulence in Enterococcus faecalis V583. Microbiology 2009; 155:3226–3237 [CrossRef][PubMed]
    [Google Scholar]
  69. Dalebroux ZD, Svensson SL, Gaynor EC, Swanson MS. ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 2010; 74:171–199 [CrossRef][PubMed]
    [Google Scholar]
  70. Schofield WB, Zimmermann-Kogadeeva M, Zimmermann M, Barry NA, Goodman AL. The stringent response determines the ability of a commensal bacterium to survive starvation and to persist in the gut. Cell Host Microbe 2018; 24:120–132 [CrossRef][PubMed]
    [Google Scholar]
  71. Ramabhadran TV, Jagger J. Mechanism of growth delay induced in Escherichia coli by near ultraviolet radiation. Proc Natl Acad Sci USA 1976; 73:59–63 [CrossRef]
    [Google Scholar]
  72. Cashel M, Gentry DR, Hernandez VJ, Vinella D. The stringent response. In Neidhardt FC. ed Escherichia coli and Salmonella: Cellular and Molecular Biology Washington, DC: American Society for Microbiology; 1996 pp 1458–1496
    [Google Scholar]
  73. Gao Q, Garcia-Pichel F. Microbial ultraviolet sunscreens. Nat Rev Microbiol 2011; 9:791–802 [CrossRef][PubMed]
    [Google Scholar]
  74. Polo A, Diamanti MV, Bjarnsholt T, Høiby N, Villa F et al. Effects of photoactivated titanium dioxide nanopowders and coating on planktonic and biofilm growth of Pseudomonas aeruginosa . Photochem Photobiol 2011; 87:1387–1394 [CrossRef][PubMed]
    [Google Scholar]
  75. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 2001; 67:1865–1873 [CrossRef][PubMed]
    [Google Scholar]
  76. De Kievit TR, Iglewski BH. Bacterial quorum sensing in pathogenic relationships. Infect Immun 2000; 68:4839–4849 [CrossRef][PubMed]
    [Google Scholar]
  77. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001; 55:165–199 [CrossRef][PubMed]
    [Google Scholar]
  78. Branda SS, Vik A, Friedman L, Kolter R. Biofilms: the matrix revisited. Trends Microbiol 2005; 13:20–26
    [Google Scholar]
  79. Ma L, Conover M, Lu H, Parsek MR, Bayles K et al. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 2009; 5:e1000354
    [Google Scholar]
  80. Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 2005; 102:11076–11081 [CrossRef][PubMed]
    [Google Scholar]
  81. De Kievit TR. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 2009; 11:279–288 [CrossRef][PubMed]
    [Google Scholar]
  82. Moradali MF, Ghods S, Rehm BHA. Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 2017; 7:39 [CrossRef][PubMed]
    [Google Scholar]
  83. Potrykus K, Cashel M. (p)ppGpp: still magical?. Annu Rev Microbiol 2008; 62:35–51
    [Google Scholar]
  84. Favre A, Hajnsdorf E, Thiam K, Caldeira de Araujo A. Mutagenesis and growth delay induced in Escherichia coli by near-ultraviolet radiations. Biochimie 1985; 67:335–342
    [Google Scholar]
  85. Blondel MO, Favre A. tRNAPhe and tRNAPro are the near-ultraviolet molecular targets triggering the growth delay effect. Biochem Biophys Res Commun 1988; 150:979–986 [CrossRef][PubMed]
    [Google Scholar]
  86. Caldeira de Araujo A, Favre A. Near ultraviolet DNA damage induces the SOS responses in Escherichia coli . EMBO J 1986; 5:175–179 [CrossRef]
    [Google Scholar]
  87. Baysse C, Cullinane M, Dénervaud V, Burrowes E, Dow JM et al. Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 2005; 151:2529–2542 [CrossRef][PubMed]
    [Google Scholar]
  88. Strempel N, Nusser M, Neidig A, Brenner-Weiss G, Overhage J. The oxidative stress agent hypochlorite stimulates c-di-GMP synthesis and biofilm formation in Pseudomonas aeruginosa . Front Microbiol 2017; 8:2311 [CrossRef][PubMed]
    [Google Scholar]
  89. Ha D-G, O'Toole GA. c-di-GMP and its effects on biofilm formation and dispersion: a Pseudomonas aeruginosa review. Microbiol Spectr 2015; 3:MB-0003-2014 [CrossRef][PubMed]
    [Google Scholar]
  90. Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 1985; 27:619–624
    [Google Scholar]
  91. Mansouri H, Alavi SA, Yari M. A study of Pseudomonas aeruginosa bacteria in microbial corrosion. 2nd International Conference on Chemical, Ecology and Environmental Sciences (ICCEES’2012) 28–29 April 2012Singapore
    [Google Scholar]
  92. Holloway BW. Genetic recombination in Pseudomonas aeruginosa . J Gen Microbiol 1955; 13:572–581 [CrossRef][PubMed]
    [Google Scholar]
  93. Pearson JP, Pesci EC, Iglewski BH. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 1997; 179:5756–5767 [CrossRef][PubMed]
    [Google Scholar]
  94. Brint JM, Ohman DE. 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; 177:7155–7163 [CrossRef][PubMed]
    [Google Scholar]
  95. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2003; 100:14339–14344 [CrossRef][PubMed]
    [Google Scholar]
  96. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ et al. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 2010; 75:827–842 [CrossRef][PubMed]
    [Google Scholar]
  97. Kirisits MJ, Prost L, Starkey M, Parsek MR. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2005; 71:4809–4821
    [Google Scholar]
  98. Wang EW, Jung JY, Pashia ME, Nason R, Scholnick S et al. Otopathogenic Pseudomonas aeruginosa strains as competent biofilm formers. Arch Otolaryngol Head Neck Surg 2005; 131:983–989 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000932
Loading
/content/journal/micro/10.1099/mic.0.000932
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