Journal of Microbiology

, Volume 56, Issue 7, pp 449–457 | Cite as

Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa

  • Donghoon Kang
  • Natalia V. Kirienko


Bacterial biofilms remain a persistent threat to human healthcare due to their role in the development of antimicrobial resistance. To combat multi-drug resistant pathogens, it is crucial to enhance our understanding of not only the regulation of biofilm formation, but also its contribution to bacterial virulence. Iron acquisition lies at the crux of these two subjects. In this review, we discuss the role of iron acquisition in biofilm formation and how hosts impede this mechanism to defend against pathogens. We also discuss recent findings that suggest that biofilm formation can also have the reciprocal effect, influencing siderophore production and iron sequestration.


iron acquisition biofilm nutritional immunity siderophore exopolysaccharides Pseudomonas aeruginosa 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alhede, M., Bjarnsholt, T., Givskov, M., and Alhede, M. 2014 Pseudomonas aeruginosa biofilms: mechanisms of immune evasion. Adv. Appl. Microbiol. 86, 1–40PubMedCrossRefGoogle Scholar
  2. Anderson, G.G. and O’Toole, G.A. 2008 Innate and induced resistance mechanisms of bacterial biofilms. Curr. Top. Microbiol. Immunol. 322, 85–105PubMedGoogle Scholar
  3. Ardehali, R., Shi, L., Janatova, J., Mohammad, S.F., and Burns, G.L. 2002 The effect of apo-transferrin on bacterial adhesion to biomaterials. Artif. Organs 26, 512–520PubMedCrossRefGoogle Scholar
  4. Bachman, M.A., Oyler, J.E., Burns, S.H., Caza, M., Lepine, F., Dozois, C.M., and Weiser, J.N. 2011 Klebsiella pneumoniae yersiniabactin promotes respiratory tract infection through evasion of lipocalin 2 Infect. Immun. 79, 3309–3316Google Scholar
  5. Baldi, F., Marchetto, D., Battistel, D., Daniele, S., Faleri, C., De Castro, C., and Lanzetta, R. 2009 Iron-binding characterization and polysaccharide production by Klebsiella oxytoca strain isolated from mine acid drainage. J. Appl. Microbiol. 107, 1241–1250PubMedPubMedCentralCrossRefGoogle Scholar
  6. Banin, E., Brady, K.M., and Greenberg, E.P. 2006 Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl. Environ. Microbiol. 72, 2064–2069PubMedPubMedCentralCrossRefGoogle Scholar
  7. Banin, E., Lozinski, A., Brady, K.M., Berenshtein, E., Butterfield, P.W., Moshe, M., Chevion, M., and Greenberg, E.P. 2008 The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc. Natl. Acad. Sci. USA 105, 16761–16766PubMedPubMedCentralCrossRefGoogle Scholar
  8. Banin, E., Vasil, M.L., and Greenberg, E.P. 2005 Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA 102, 11076–11081PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beddek, A.J. and Schryvers, A.B. 2010 The lactoferrin receptor complex in Gram negative bacteria. Biometals 23, 377–386PubMedCrossRefGoogle Scholar
  10. Berger, T., Togawa, A., Duncan, G.S., Elia, A.J., You-Ten, A., Wakeham, A., Fong, H.E., Cheung, C.C., and Mak, T.W. 2006 Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA 103, 1834–1839PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bernardini, M.L., Sanna, M.G., Fontaine, A., and Sansonetti, P.J. 1993 OmpC is involved in invasion of epithelial cells by Shigella flexneri. Infect. Immun. 61, 3625–3635PubMedPubMedCentralGoogle Scholar
  12. Boyce, J.R. and Miller, R.V. 1980 Effects of cations on stability of cystic fibrosis associated mucoid Pseudomonas. Lancet 2, 268–269PubMedCrossRefGoogle Scholar
  13. Boyce, J.R. and Miller, R.V. 1982 Selection of nonmucoid derivatives of mucoid Pseudomonas aeruginosa is strongly influenced by the level of iron in the culture medium. Infect. Immun. 37, 695–701PubMedPubMedCentralGoogle Scholar
  14. Bridier, A., Dubois-Brissonnet, F., Boubetra, A., Thomas, V., and Briandet, R. 2010 The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J. Microbiol. Methods 82, 64–70PubMedCrossRefGoogle Scholar
  15. Cady, N.C., McKean, K.A., Behnke, J., Kubec, R., Mosier, A.P., Kasper, S.H., Burz, D.S., and Musah, R.A. 2012 Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS One 7, e38492PubMedPubMedCentralCrossRefGoogle Scholar
  16. Camilli, A. and Bassler, B.L. 2006 Bacterial small-molecule signaling pathways. Science 311, 1113–1116PubMedPubMedCentralCrossRefGoogle Scholar
  17. Carrano, C.J. and Raymond, K.N. 1979 Ferric ion sequestering agents. 2 Kinetics and mechanism of iron removal from transferrin by enterobactin and synthetic tricatechols. J. Am. Chem. Soc. 101, 5401–5404Google Scholar
  18. Carver, P.L. 2018 The battle for iron between humans and microbes. Curr. Med. Chem. 25, 85–96PubMedCrossRefGoogle Scholar
  19. Cescau, S., Cwerman, H., Letoffe, S., Delepelaire, P., Wandersman, C., and Biville, F. 2007 Heme acquisition by hemophores. Biometals 20, 603–613PubMedCrossRefGoogle Scholar
  20. Chitambar, C.R. and Narasimhan, J. 1991 Targeting iron-dependent DNA synthesis with gallium and transferrin-gallium. Pathobiology 59, 3–10PubMedCrossRefGoogle Scholar
  21. Colvin, K.M., Gordon, V.D., Murakami, K., Borlee, B.R., Wozniak, D.J., Wong, G.C., and Parsek, M.R. 2011 The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog. 7, e1001264PubMedPubMedCentralCrossRefGoogle Scholar
  22. Colvin, K.M., Irie, Y., Tart, C.S., Urbano, R., Whitney, J.C., Ryder, C., Howell, P.L., Wozniak, D.J., and Parsek, M.R. 2012 The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol. 14, 1913–1928PubMedCrossRefGoogle Scholar
  23. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. 1999 Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322PubMedCrossRefGoogle Scholar
  24. De Philippis, R., Colica, G., and Micheletti, E. 2011 Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process. Appl. Microbiol. Biotechnol. 92, 697–708PubMedCrossRefGoogle Scholar
  25. Donlan, R.M. 2002 Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8, 881–890PubMedPubMedCentralCrossRefGoogle Scholar
  26. Drenkard, E. and Ausubel, F.M. 2002 Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416, 740–743PubMedCrossRefGoogle Scholar
  27. Ferreira, J.A., Penner, J.C., Moss, R.B., Haagensen, J.A., Clemons, K.V., Spormann, A.M., Nazik, H., Cohen, K., Banaei, N., Carolino, E., et al. 2015 Inhibition of Aspergillus fumigatus and its biofilm by Pseudomonas aeruginosa is dependent on the source, phenotype and growth conditions of the bacterium. PLoS One 10, e0134692PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fischbach, M.A., Lin, H., Zhou, L., Yu, Y., Abergel, R.J., Liu, D.R., Raymond, K.N., Wanner, B.L., Strong, R.K., Walsh, C.T., et al. 2006 The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2 Proc. Natl. Acad. Sci. USA 103, 16502–16507CrossRefGoogle Scholar
  29. Flemming, H.C. and Wingender, J. 2010 The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633PubMedCrossRefGoogle Scholar
  30. Flo, T.H., Smith, K.D., Sato, S., Rodriguez, D.J., Holmes, M.A., Strong, R.K., Akira, S., and Aderem, A. 2004 Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917–921PubMedCrossRefGoogle Scholar
  31. Franklin, M.J., Nivens, D.E., Weadge, J.T., and Howell, P.L. 2011 Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front. Microbiol. 2, 167PubMedPubMedCentralCrossRefGoogle Scholar
  32. Friedman, L. and Kolter, R. 2004 Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186, 4457–4465PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gilbert, P., Jones, M.V., Allison, D.G., Heys, S., Maira, T., and Wood, P. 1998 The use of poloxamer hydrogels for the assessment of biofilm susceptibility towards biocide treatments. J. Appl. Microbiol. 85, 985–990PubMedCrossRefGoogle Scholar
  34. Goetz, D.H., Holmes, M.A., Borregaard, N., Bluhm, M.E., Raymond, K.N., and Strong, R.K. 2002 The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell 10, 1033–1043PubMedCrossRefGoogle Scholar
  35. Goodman, A.L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R.S., and Lory, S. 2004 A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7, 745–754PubMedCrossRefGoogle Scholar
  36. Gupta, P. and Diwan, B. 2017 Bacterial exopolysaccharide mediated heavy metal removal: A Review on biosynthesis, mechanism and remediation strategies. Biotechnol. Rep. (Amst) 13, 58–71CrossRefGoogle Scholar
  37. Guterman, S.K., Morris, P.M., and Tannenberg, W.J. 1978 Feasibility of enterochelin as an iron-chelating drug: studies with human serum and a mouse model system. Gen. Pharmacol. 9, 123–127PubMedCrossRefGoogle Scholar
  38. Hall-Stoodley, L., Costerton, J.W., and Stoodley, P. 2004 Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108PubMedCrossRefGoogle Scholar
  39. Harris, W.R., Carrano, C.J., and Raymond, K.N. 1979 Isolation, characterization, and formation constants of ferric aerobactin. J. Am. Chem. Soc. 101, 2722–2727CrossRefGoogle Scholar
  40. Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., Kumar, N., Schembri, M.A., Song, Z., Kristoffersen, P., et al. 2003 Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803–3815PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hoiby, N., Krogh Johansen, H., Moser, C., Song, Z., Ciofu, O., and Kharazmi, A. 2001 Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect. 3, 23–35PubMedCrossRefGoogle Scholar
  42. Hood, M.I. and Skaar, E.P. 2012 Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525–537PubMedCrossRefGoogle Scholar
  43. Huang, W. and Wilks, A. 2017 Extracellular heme uptake and the challenge of bacterial cell membranes. Annu. Rev. Biochem. 86, 799–823PubMedCrossRefGoogle Scholar
  44. Hunter, R.C., Asfour, F., Dingemans, J., Osuna, B.L., Samad, T., Malfroot, A., Cornelis, P., and Newman, D.K. 2013 Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. MBio 4, e00557-13PubMedPubMedCentralCrossRefGoogle Scholar
  45. Irie, Y., Borlee, B.R., O’Connor, J.R., Hill, P.J., Harwood, C.S., Wozniak, D.J., and Parsek, M.R. 2012 Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 109, 20632–20636PubMedPubMedCentralCrossRefGoogle Scholar
  46. Javvadi, S., Pandey, S.S., Mishra, A., Pradhan, B.B., and Chatterjee, S. 2018 Bacterial cyclic ß-(1,2)-glucans sequester iron to protect against iron-induced toxicity. EMBO Rep. 19, 172–186PubMedCrossRefGoogle Scholar
  47. Jayaraman, R. 2008 Bacterial persistence: some new insights into an old phenomenon. J. Biosci. 33, 795–805PubMedCrossRefGoogle Scholar
  48. Jensen, E.T., Kharazmi, A., Lam, K., Costerton, J.W., and Hoiby, N. 1990 Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms. Infect. Immun. 58, 2383–2385PubMedPubMedCentralGoogle Scholar
  49. Kamiya, H., Ehara, T., and Matsumoto, T. 2012 Inhibitory effects of lactoferrin on biofilm formation in clinical isolates of Pseudomonas aeruginosa. J. Infect. Chemother. 18, 47–52PubMedCrossRefGoogle Scholar
  50. Kaneko, Y., Thoendel, M., Olakanmi, O., Britigan, B.E., and Singh, P.K. 2007 The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117, 877–888PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kang, D., Kirienko, D.R., Webster, P., Fisher, A.L., and Kirienko, N.V. 2018 Pyoverdine, a siderophore from Pseudomonas aeruginosa, translocates into C. elegans, removes iron, and activates a distinct host response. Virulence 9, 804–817PubMedGoogle Scholar
  52. Kang, D. and Kirienko, N.V. 2017 High-throughput genetic screen reveals that early attachment and biofilm formation are necessary for full pyoverdine production by Pseudomonas aeruginosa. Front. Microbiol. 8, 1707PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kang, D., Turner, K.E., and Kirienko, N.V. 2017 PqsA promotes pyoverdine production via biofilm formation. Pathogens 7, 3PubMedCentralCrossRefGoogle Scholar
  54. Kelson, A.B., Carnevali, M., and Truong-Le, V. 2013 Gallium-based anti-infectives: targeting microbial iron-uptake mechanisms. Curr. Opin. Pharmacol. 13, 707–716PubMedCrossRefGoogle Scholar
  55. Kester, J.C. and Fortune, S.M. 2014 Persisters and beyond: mechanisms of phenotypic drug resistance and drug tolerance in bacteria. Crit. Rev. Biochem. Mol. Biol. 49, 91–101PubMedCrossRefGoogle Scholar
  56. Kim, S.K. and Lee, J.H. 2016 Biofilm dispersion in Pseudomonas aeruginosa. J. Microbiol. 54, 71–85PubMedCrossRefGoogle Scholar
  57. Kirienko, N.V., Ausubel, F.M., and Ruvkun, G. 2015 Mitophagy confers resistance to siderophore-mediated killing by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 112, 1821–1826PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kirienko, N.V., Kirienko, D.R., Larkins-Ford, J., Wählby, C., Ruvkun, G., and Ausubel, F.M. 2013 Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death. Cell Host Microbe 13, 406–416PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kirov, S.M., Webb, J.S., O’May, C.Y., Reid, D.W., Woo, J.K., Rice, S.A., and Kjelleberg, S. 2007 Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 153, 3264–3274PubMedCrossRefGoogle Scholar
  60. Komor, U., Bielecki, P., Loessner, H., Rohde, M., Wolf, K., Westphal, K., Weiss, S., and Haussler, S. 2012 Biofilm formation by Pseudomonas aeruginosa in solid murine tumors-a novel model system. Microbes Infect. 14, 951–958PubMedCrossRefGoogle Scholar
  61. Kostenko, V., Ceri, H., and Martinuzzi, R.J. 2007 Increased tolerance of Staphylococcus aureus to vancomycin in viscous media. FEMS Immun. Med. Microbiol. 51, 277–288CrossRefGoogle Scholar
  62. Kragh, K.N., Alhede, M., Rybtke, M., Stavnsberg, C., Jensen, P.O., Tolker-Nielsen, T., Whiteley, M., and Bjarnsholt, T. 2018 Inoculation method could impact the outcome of microbiological experiments. Appl. Environ. Microbiol. 84, e02264-17PubMedCentralGoogle Scholar
  63. Kvach, J.T., Wiles, T.I., Mellencamp, M.W., and Kochan, I. 1977 Use of transferrin-iron enterobactin complexes as the source of iron by serum-exposed bacteria. Infect. Immun. 18, 439–445PubMedPubMedCentralGoogle Scholar
  64. Lamont, I.L., Beare, P.A., Ochsner, U., Vasil, A.I., and Vasil, M.L. 2002 Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 99, 7072–7077PubMedPubMedCentralCrossRefGoogle Scholar
  65. Leid, J.G., Willson, C.J., Shirtliff, M.E., Hassett, D.J., Parsek, M.R., and Jeffers, A.K. 2005 The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gammamediated macrophage killing. J. Immun. 175, 7512–7518PubMedCrossRefGoogle Scholar
  66. Li, X.H. and Lee, J.H. 2017 Antibiofilm agents: A new perspective for antimicrobial strategy. J. Microbiol. 55, 753–766PubMedCrossRefGoogle Scholar
  67. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J. 2009 Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog. 5, e1000354PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ma, L., Jackson, K.D., Landry, R.M., Parsek, M.R., and Wozniak, D.J. 2006 Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J. Bacteriol. 188, 8213–8221PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mah, T.F. and O’Toole, G.A. 2001 Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34–39PubMedCrossRefGoogle Scholar
  70. Meyer, J.M., Neely, A., Stintzi, A., Georges, C., and Holder, I.A. 1996 Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect. Immun. 64, 518–523PubMedPubMedCentralGoogle Scholar
  71. Mikkelsen, H., Sivaneson, M., and Filloux, A. 2011 Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ. Microbiol. 13, 1666–1681PubMedCrossRefGoogle Scholar
  72. Miller, R.V. and Rubero, V.J. 1984 Mucoid conversion by phages of Pseudomonas aeruginosa strains from patients with cystic fibrosis. J. Clin. Microbiol. 19, 717–719PubMedPubMedCentralGoogle Scholar
  73. Minandri, F., Imperi, F., Frangipani, E., Bonchi, C., Visaggio, D., Facchini, M., Pasquali, P., Bragonzi, A., and Visca, P. 2016 Role of iron uptake systems in Pseudomonas aeruginosa virulence and airway infection. Infect. Immun. 84, 2324–2335PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mohite, B.V., Koli, S.H., Narkhede, C.P., Patil, S.N., and Patil, S.V. 2017 Prospective of microbial exopolysaccharide for heavy metal exclusion. Appl. Biochem. Biotechnol. 183, 582–600PubMedCrossRefGoogle Scholar
  75. Moppert, X., Le Costaouec, T., Raguenes, G., Courtois, A., Simon-Colin, C., Crassous, P., Costa, B., and Guezennec, J. 2009 Investigations into the uptake of copper, iron and selenium by a highly sulphated bacterial exopolysaccharide isolated from microbial mats. J. Ind. Microbiol. Biotechnol. 36, 599–604PubMedCrossRefGoogle Scholar
  76. Moradali, M.F., Ghods, S., and Rehm, B.H. 2017 Pseudomonas aeruginosa lifestyle: A paradigm for adaptation, survival, and persistence. Front. Cell. Infect. Microbiol. 7, 39PubMedPubMedCentralCrossRefGoogle Scholar
  77. Moreau-Marquis, S., Bomberger, J.M., Anderson, G.G., Swiatecka-Urban, A., Ye, S., O’Toole, G.A., and Stanton, B.A. 2008 The F508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am. J. Physiol. Lung Cell. Mol. Physiol. 295 L25–L37PubMedPubMedCentralCrossRefGoogle Scholar
  78. Moreau-Marquis, S., O’Toole, G.A., and Stanton, B.A. 2009 Tobra mycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am. J. Respir. Cell Mol. Biol. 41, 305–313PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. 2008 Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213PubMedPubMedCentralCrossRefGoogle Scholar
  80. O’Loughlin, C.T., Miller, L.C., Siryaporn, A., Drescher, K., Semmelhack, M.F., and Bassler, B.L. 2013 A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl. Acad. Sci. USA 110, 17981–17986PubMedPubMedCentralCrossRefGoogle Scholar
  81. O’May, C.Y., Sanderson, K., Roddam, L.F., Kirov, S.M., and Reid, D.W. 2009 Iron-binding compounds impair Pseudomonas aeruginosa biofilm formation, especially under anaerobic conditions. J. Med. Microbiol. 58, 765–773PubMedCrossRefGoogle Scholar
  82. Oglesby-Sherrouse, A.G., Djapgne, L., Nguyen, A.T., Vasil, A.I., and Vasil, M.L. 2014 The complex interplay of iron, biofilm formation, and mucoidy affecting antimicrobial resistance of Pseudomonas aeruginosa. Pathog. Dis. 70, 307–320PubMedPubMedCentralCrossRefGoogle Scholar
  83. Palmer, L.D. and Skaar, E.P. 2016 Transition metals and virulence in bacteria. Annu. Rev. Genet. 50, 67–91PubMedPubMedCentralCrossRefGoogle Scholar
  84. Parsek, M.R. and Greenberg, E.P. 2000 Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 97, 8789–8793PubMedPubMedCentralCrossRefGoogle Scholar
  85. Peek, M.E., Bhatnagar, A., McCarty, N.A., and Zughaier, S.M. 2012 Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdiscip. Perspect. Infect. Dis. 2012, 843509PubMedPubMedCentralCrossRefGoogle Scholar
  86. Penner, J.C., Ferreira, J.A., Secor, P.R., Sweere, J.M., Birukova, M.K., Joubert, L.M., Haagensen, J.A., Garcia, O., Malkovskiy, A.V., Kaber, G., et al. 2016 Pf4 bacteriophage produced by Pseudomonas aeruginosa inhibits Aspergillus fumigatus metabolism via iron sequestration. Microbiology 162, 1583–1594PubMedCrossRefGoogle Scholar
  87. Petrova, O.E. and Sauer, K. 2009 A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog. 5, e1000668PubMedPubMedCentralCrossRefGoogle Scholar
  88. Peyton, B.M. 1996 Effects of shear stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density. Wat. Res. 30, 29–36CrossRefGoogle Scholar
  89. Peyton, B.M. and Characklis, W.G. 1993 A statistical analysis of the effect of substrate utilization and shear stress on the kinetics of biofilm detachment. Biotechnol. Bioeng. 41, 728–735PubMedCrossRefGoogle Scholar
  90. Pogoutse, A.K. and Moraes, T.F. 2017 Iron acquisition through the bacterial transferrin receptor. Crit. Rev. Biochem. Mol. Biol. 52, 314–326PubMedCrossRefGoogle Scholar
  91. Rashid, M.H., Rumbaugh, K., Passador, L., Davies, D.G., Hamood, A.N., Iglewski, B.H., and Kornberg, A. 2000 Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97, 9636–9641PubMedPubMedCentralCrossRefGoogle Scholar
  92. Rasmussen, B. 2000 Filamentous microfossils in a 3,235-millionyear-old volcanogenic massive sulphide deposit. Nature 405, 676–679PubMedCrossRefGoogle Scholar
  93. Rice, S.A., Tan, C.H., Mikkelsen, P.J., Kung, V., Woo, J., Tay, M., Hauser, A., McDougald, D., Webb, J.S., and Kjelleberg, S. 2009 The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 3, 271–282PubMedCrossRefGoogle Scholar
  94. Rittman, B.E. 1982 The effect of shear stress on biofilm loss rate. Biotechnol. Bioeng. 24, 501–506PubMedCrossRefGoogle Scholar
  95. Ruhs, P.A., Boni, L., Fuller, G.G., Inglis, R.F., and Fischer, P. 2013 In situ quantification of the interfacial rheological response of bacterial biofilms to environmental stimuli. PLoS One 8, e78524PubMedPubMedCentralCrossRefGoogle Scholar
  96. Sakuragi, Y. and Kolter, R. 2007 Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J. Bacteriol. 189, 5383–5386PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W., and Davies, D.G. 2002 Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140–1154PubMedPubMedCentralCrossRefGoogle Scholar
  98. She, P., Chen, L., Qi, Y., Xu, H., Liu, Y., Wang, Y., Luo, Z., and Wu, Y. 2016 Effects of human serum and apo-transferrin on Staphylococcus epidermidis RP62A biofilm formation. Microbiologyopen 5, 957–966PubMedPubMedCentralCrossRefGoogle Scholar
  99. Shih, P.C. and Huang, C.T. 2002 Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. J. Antimicrob. Chemother. 49, 309–314PubMedCrossRefGoogle Scholar
  100. Singh, P.K., Parsek, M.R., Greenberg, E.P., and Welsh, M.J. 2002 A component of innate immunity prevents bacterial biofilm development. Nature 417, 552–555PubMedCrossRefGoogle Scholar
  101. Singh, P.K., Schaefer, A.L., Parsek, M.R., Moninger, T.O., Welsh, M.J., and Greenberg, E.P. 2000 Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407, 762–764PubMedCrossRefGoogle Scholar
  102. Skaar, E.P. 2010 The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog. 6, e1000949PubMedPubMedCentralCrossRefGoogle Scholar
  103. Stewart, P.S. 1996 Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40, 2517–2522PubMedPubMedCentralCrossRefGoogle Scholar
  104. Stoodley, P., Sauer, K., Davies, D.G., and Costerton, J.W. 2002 Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209PubMedCrossRefGoogle Scholar
  105. Takase, H., Nitanai, H., Hoshino, K., and Otani, T. 2000 Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68, 1834–1839PubMedPubMedCentralCrossRefGoogle Scholar
  106. Terry, J.M., Pina, S.E., and Mattingly, S.J. 1992 Role of energy metabolism in conversion of nonmucoid Pseudomonas aeruginosa to the mucoid phenotype. Infect. Immun. 60, 1329–1335PubMedPubMedCentralGoogle Scholar
  107. Tidmarsh, G.F., Klebba, P.E., and Rosenberg, L.T. 1983 Rapid release of iron from ferritin by siderophores. J. Inorg. Biochem. 18, 161–168PubMedCrossRefGoogle Scholar
  108. Valdebenito, M., Muller, S.I., and Hantke, K. 2007 Special conditions allow binding of the siderophore salmochelin to siderocalin (NGAL-lipocalin). FEMS Microbiol. Lett. 277, 182–187PubMedCrossRefGoogle Scholar
  109. Visaggio, D., Pasqua, M., Bonchi, C., Kaever, V., Visca, P., and Imperi, F. 2015 Cell aggregation promotes pyoverdine-dependent iron uptake and virulence in Pseudomonas aeruginosa. Front. Microbiol. 6, 902PubMedPubMedCentralCrossRefGoogle Scholar
  110. Vogeleer, P., Tremblay, Y.D., Mafu, A.A., Jacques, M., and Harel, J. 2014 Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front. Microbiol. 5, 317PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wakabayashi, H., Yamauchi, K., Kobayashi, T., Yaeshima, T., Iwatsuki, K., and Yoshie, H. 2009 Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia. Antimicrob. Agents Chemother. 53, 3308–3316PubMedPubMedCentralCrossRefGoogle Scholar
  112. Webb, J.S., Lau, M., and Kjelleberg, S. 2004 Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186, 8066–8073PubMedPubMedCentralCrossRefGoogle Scholar
  113. Webb, J.S., Thompson, L.S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., Givskov, M., and Kjelleberg, S. 2003 Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, 4585–4592PubMedPubMedCentralCrossRefGoogle Scholar
  114. Whiteley, M., Bangera, M.G., Bumgarner, R.E., Parsek, M.R., Teitzel, G.M., Lory, S., and Greenberg, E.P. 2001 Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860–864PubMedCrossRefGoogle Scholar
  115. Winstanley, C., O’Brien, S., and Brockhurst, M.A. 2016 Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 24, 327–337PubMedPubMedCentralCrossRefGoogle Scholar
  116. Wirtanen, G., Salo, S., Allison, D.G., Mattila-Sandholm, T., and Gilbert, P. 1998 Performance evaluation of disinfectant formulations using poloxamer-hydrogel biofilm-constructs. J. Appl. Microbiol. 85, 965–971PubMedCrossRefGoogle Scholar
  117. Wolz, C., Hohloch, K., Ocaktan, A., Poole, K., Evans, R.W., Rochel, N., Albrecht-Gary, A.M., Abdallah, M.A., and Döring, G. 1994 Iron release from transferrin by pyoverdin and elastase from Pseudomonas aeruginosa. Infect. Immun. 62, 4021–4027PubMedPubMedCentralGoogle Scholar
  118. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K.C., Birrer, P., Bellon, G., Berger, J., Weiss, T., et al. 2002 Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109, 317–325PubMedPubMedCentralCrossRefGoogle Scholar
  119. Xiao, R. and Kisaalita, W.S. 1997 Iron acquisition from transferrin and lactoferrin by Pseudomonas aeruginosa pyoverdin. Microbiology 143 (Pt 7). 2509–2515PubMedCrossRefGoogle Scholar
  120. Yoon, S.S., Hennigan, R.F., Hilliard, G.M., Ochsner, U.A., Parvatiyar, K., Kamani, M.C., Allen, H.L., DeKievit, T.R., Gardner, P.R., Schwab, U., et al. 2002 Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell. 3, 593–603PubMedCrossRefGoogle Scholar
  121. Yu, S., Wei, Q., Zhao, T., Guo, Y., and Ma, L.Z. 2016 A survival strategy for Pseudomonas aeruginosa that uses exopolysaccharides to sequester and store iron to stimulate Psl-dependent biofilm formation. Appl. Environ. Microbiol. 82, 6403–6413PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of BiosciencesRice UniversityHoustonUSA

Personalised recommendations