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Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa

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Abstract

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.

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References

  • Alhede, M., Bjarnsholt, T., Givskov, M., and Alhede, M. 2014 Pseudomonas aeruginosa biofilms: mechanisms of immune evasion. Adv. Appl. Microbiol. 86, 1–40

    Article  PubMed  CAS  Google Scholar 

  • Anderson, G.G. and O’Toole, G.A. 2008 Innate and induced resistance mechanisms of bacterial biofilms. Curr. Top. Microbiol. Immunol. 322, 85–105

    PubMed  CAS  Google Scholar 

  • 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, 512–520

    Article  PubMed  CAS  Google Scholar 

  • 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, 3309–3316

    CAS  Google Scholar 

  • 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, 1241–1250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 2064–2069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 16761–16766

    Article  PubMed  PubMed Central  Google Scholar 

  • Banin, E., Vasil, M.L., and Greenberg, E.P. 2005 Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA 102, 11076–11081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beddek, A.J. and Schryvers, A.B. 2010 The lactoferrin receptor complex in Gram negative bacteria. Biometals 23, 377–386

    Article  PubMed  CAS  Google Scholar 

  • 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, 1834–1839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 3625–3635

    PubMed  PubMed Central  CAS  Google Scholar 

  • Boyce, J.R. and Miller, R.V. 1980 Effects of cations on stability of cystic fibrosis associated mucoid Pseudomonas. Lancet 2, 268–269

    Article  PubMed  CAS  Google Scholar 

  • 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, 695–701

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 64–70

    Article  PubMed  CAS  Google Scholar 

  • 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, e38492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Camilli, A. and Bassler, B.L. 2006 Bacterial small-molecule signaling pathways. Science 311, 1113–1116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 5401–5404

    CAS  Google Scholar 

  • Carver, P.L. 2018 The battle for iron between humans and microbes. Curr. Med. Chem. 25, 85–96

    Article  PubMed  CAS  Google Scholar 

  • Cescau, S., Cwerman, H., Letoffe, S., Delepelaire, P., Wandersman, C., and Biville, F. 2007 Heme acquisition by hemophores. Biometals 20, 603–613

    Article  PubMed  CAS  Google Scholar 

  • Chitambar, C.R. and Narasimhan, J. 1991 Targeting iron-dependent DNA synthesis with gallium and transferrin-gallium. Pathobiology 59, 3–10

    Article  PubMed  CAS  Google Scholar 

  • 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, e1001264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 1913–1928

    Article  PubMed  CAS  Google Scholar 

  • Costerton, J.W., Stewart, P.S., and Greenberg, E.P. 1999 Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322

    Article  PubMed  CAS  Google Scholar 

  • 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, 697–708

    Article  PubMed  CAS  Google Scholar 

  • Donlan, R.M. 2002 Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8, 881–890

    Article  PubMed  PubMed Central  Google Scholar 

  • Drenkard, E. and Ausubel, F.M. 2002 Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416, 740–743

    Article  PubMed  CAS  Google Scholar 

  • 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, e0134692

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 16502–16507

    Article  CAS  Google Scholar 

  • Flemming, H.C. and Wingender, J. 2010 The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633

    Article  PubMed  CAS  Google Scholar 

  • 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, 917–921

    Article  PubMed  CAS  Google Scholar 

  • 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, 167

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedman, L. and Kolter, R. 2004 Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 186, 4457–4465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 985–990

    Article  PubMed  CAS  Google Scholar 

  • 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, 1033–1043

    Article  PubMed  CAS  Google Scholar 

  • 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, 745–754

    Article  PubMed  CAS  Google Scholar 

  • Gupta, P. and Diwan, B. 2017 Bacterial exopolysaccharide mediated heavy metal removal: A Review on biosynthesis, mechanism and remediation strategies. Biotechnol. Rep. (Amst) 13, 58–71

    Article  Google Scholar 

  • 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, 123–127

    Article  PubMed  CAS  Google Scholar 

  • Hall-Stoodley, L., Costerton, J.W., and Stoodley, P. 2004 Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108

    Article  PubMed  CAS  Google Scholar 

  • Harris, W.R., Carrano, C.J., and Raymond, K.N. 1979 Isolation, characterization, and formation constants of ferric aerobactin. J. Am. Chem. Soc. 101, 2722–2727

    Article  CAS  Google Scholar 

  • 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, 3803–3815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 23–35

    Article  PubMed  CAS  Google Scholar 

  • Hood, M.I. and Skaar, E.P. 2012 Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525–537

    Article  PubMed  CAS  Google Scholar 

  • Huang, W. and Wilks, A. 2017 Extracellular heme uptake and the challenge of bacterial cell membranes. Annu. Rev. Biochem. 86, 799–823

    Article  PubMed  CAS  Google Scholar 

  • 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, e00557-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 20632–20636

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 172–186

    Article  PubMed  CAS  Google Scholar 

  • Jayaraman, R. 2008 Bacterial persistence: some new insights into an old phenomenon. J. Biosci. 33, 795–805

    Article  PubMed  CAS  Google Scholar 

  • 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, 2383–2385

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 47–52

    Article  PubMed  CAS  Google Scholar 

  • 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, 877–888

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 804–817

    PubMed  CAS  Google Scholar 

  • 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, 1707

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang, D., Turner, K.E., and Kirienko, N.V. 2017 PqsA promotes pyoverdine production via biofilm formation. Pathogens 7, 3

    Article  PubMed Central  Google Scholar 

  • Kelson, A.B., Carnevali, M., and Truong-Le, V. 2013 Gallium-based anti-infectives: targeting microbial iron-uptake mechanisms. Curr. Opin. Pharmacol. 13, 707–716

    Article  PubMed  CAS  Google Scholar 

  • 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, 91–101

    Article  PubMed  CAS  Google Scholar 

  • Kim, S.K. and Lee, J.H. 2016 Biofilm dispersion in Pseudomonas aeruginosa. J. Microbiol. 54, 71–85

    Article  PubMed  CAS  Google Scholar 

  • 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, 1821–1826

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 406–416

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 3264–3274

    Article  PubMed  CAS  Google Scholar 

  • 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, 951–958

    Article  PubMed  CAS  Google Scholar 

  • Kostenko, V., Ceri, H., and Martinuzzi, R.J. 2007 Increased tolerance of Staphylococcus aureus to vancomycin in viscous media. FEMS Immun. Med. Microbiol. 51, 277–288

    Article  CAS  Google Scholar 

  • 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, e02264-17

    PubMed Central  Google Scholar 

  • 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, 439–445

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 7072–7077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 7512–7518

    Article  PubMed  CAS  Google Scholar 

  • Li, X.H. and Lee, J.H. 2017 Antibiofilm agents: A new perspective for antimicrobial strategy. J. Microbiol. 55, 753–766

    Article  PubMed  CAS  Google Scholar 

  • 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, e1000354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 8213–8221

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mah, T.F. and O’Toole, G.A. 2001 Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34–39

    Article  PubMed  CAS  Google Scholar 

  • 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, 518–523

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mikkelsen, H., Sivaneson, M., and Filloux, A. 2011 Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ. Microbiol. 13, 1666–1681

    Article  PubMed  CAS  Google Scholar 

  • 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, 717–719

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 2324–2335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 582–600

    Article  PubMed  CAS  Google Scholar 

  • 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, 599–604

    Article  PubMed  CAS  Google Scholar 

  • 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, 39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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–L37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 305–313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. 2008 Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 17981–17986

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 765–773

    Article  PubMed  CAS  Google Scholar 

  • 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, 307–320

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer, L.D. and Skaar, E.P. 2016 Transition metals and virulence in bacteria. Annu. Rev. Genet. 50, 67–91

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 8789–8793

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 843509

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 1583–1594

    Article  PubMed  CAS  Google Scholar 

  • Petrova, O.E. and Sauer, K. 2009 A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog. 5, e1000668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peyton, B.M. 1996 Effects of shear stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density. Wat. Res. 30, 29–36

    Article  CAS  Google Scholar 

  • 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, 728–735

    Article  PubMed  CAS  Google Scholar 

  • Pogoutse, A.K. and Moraes, T.F. 2017 Iron acquisition through the bacterial transferrin receptor. Crit. Rev. Biochem. Mol. Biol. 52, 314–326

    Article  PubMed  CAS  Google Scholar 

  • 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, 9636–9641

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rasmussen, B. 2000 Filamentous microfossils in a 3,235-millionyear-old volcanogenic massive sulphide deposit. Nature 405, 676–679

    Article  PubMed  CAS  Google Scholar 

  • 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, 271–282

    Article  PubMed  CAS  Google Scholar 

  • Rittman, B.E. 1982 The effect of shear stress on biofilm loss rate. Biotechnol. Bioeng. 24, 501–506

    Article  PubMed  CAS  Google Scholar 

  • 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, e78524

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakuragi, Y. and Kolter, R. 2007 Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J. Bacteriol. 189, 5383–5386

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 1140–1154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 957–966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 309–314

    Article  PubMed  CAS  Google Scholar 

  • 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, 552–555

    Article  PubMed  CAS  Google Scholar 

  • 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, 762–764

    Article  PubMed  CAS  Google Scholar 

  • Skaar, E.P. 2010 The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog. 6, e1000949

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stewart, P.S. 1996 Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40, 2517–2522

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stoodley, P., Sauer, K., Davies, D.G., and Costerton, J.W. 2002 Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209

    Article  PubMed  CAS  Google Scholar 

  • Takase, H., Nitanai, H., Hoshino, K., and Otani, T. 2000 Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68, 1834–1839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 1329–1335

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tidmarsh, G.F., Klebba, P.E., and Rosenberg, L.T. 1983 Rapid release of iron from ferritin by siderophores. J. Inorg. Biochem. 18, 161–168

    Article  PubMed  CAS  Google Scholar 

  • 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, 182–187

    Article  PubMed  CAS  Google Scholar 

  • 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, 902

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 317

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 3308–3316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Webb, J.S., Lau, M., and Kjelleberg, S. 2004 Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186, 8066–8073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 4585–4592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 860–864

    Article  PubMed  CAS  Google Scholar 

  • 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, 327–337

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 965–971

    Article  PubMed  CAS  Google Scholar 

  • 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, 4021–4027

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 317–325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao, R. and Kisaalita, W.S. 1997 Iron acquisition from transferrin and lactoferrin by Pseudomonas aeruginosa pyoverdin. Microbiology 143 (Pt 7). 2509–2515

    Article  PubMed  CAS  Google Scholar 

  • 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, 593–603

    Article  PubMed  CAS  Google Scholar 

  • 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, 6403–6413

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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  1. Department of Biosciences, Rice University, Houston, USA

    Donghoon Kang & Natalia V. Kirienko

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Kang, D., Kirienko, N.V. Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa. J Microbiol. 56, 449–457 (2018). https://doi.org/10.1007/s12275-018-8114-3

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