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Review Articles

Iron metabolism in Pseudomonas aeruginosa biofilm and the involved iron-targeted anti-biofilm strategies

ORCID Icon, , &
Pages 249-258 | Received 22 May 2020, Accepted 12 Sep 2020, Published online: 07 Oct 2020

References

  • Zhang Y, Pan X, Liao S, et al. Quantitative proteomics reveals the mechanism of silver nanoparticles against multidrug-resistant Pseudomonas aeruginosa biofilms. J Proteome Res. 2020;19(8):3109–3122.
  • Richter K, Thomas N, Claeys J, et al. A topical hydrogel with deferiprone and gallium-protoporphyrin targets bacterial iron metabolism and has antibiofilm activity. Antimicrob Agents Chemother. 2017;61(6):e00481–17.
  • Nathwani D, Raman G, Sulham K, et al. Clinical and economic consequences of hospital-acquired resistant and multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2014;3(1):32.
  • Skariyachan S, Sridhar VS, Packirisamy S, et al. Recent perspectives on the molecular basis of biofilm formation by Pseudomonas aeruginosa and approaches for treatment and biofilm dispersal. Folia Microbiol. 2018;63(4):413–432.
  • Thaden JT, Park LP, Maskarinec SA, et al. Results from a 13-year prospective cohort study show increased mortality associated with bloodstream infections caused by Pseudomonas aeruginosa compared to other bacteria. Antimicrob Agents Chemother. 2017;61(6):e02671–16.
  • Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2(2):95–108.
  • Andrews SC, Robinson AK, Rodríguez-Quiñones F. Bacterial iron homeostasis. FEMS Microbiol Rev. 2003;27(2-3):215–237.
  • Saha M, Sarkar S, Sarkar B, et al. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int. 2016;23(5):3984–3999.
  • Singh PK, Parsek MR, Greenberg EP, et al. A component of innate immunity prevents bacterial biofilm development. Nature. 2002;417(6888):552–555.
  • Berlutti F, Morea C, Battistoni A, et al. Iron availability influences aggregation, biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderia cenocepacia. Int J Immunopathol Pharmacol. 2005;18(4):661–670.
  • Hider RC, Kong X. Chemistry and biology of siderophores. Nat Prod Rep. 2010;27(5):637–657.
  • Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA. 2005;102(31):11076–11081.
  • Ochsner UA, Johnson Z, Lamont IL, et al. Exotoxin A production in Pseudomonas aeruginosa requires the iron-regulated pvdS gene encoding an alternative sigma factor. Mol Microbiol. 1996;21(5):1019–1028.
  • Wilderman PJ, Vasil AI, Johnson Z, et al. Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa. Infect Immun. 2001;69(9):5385–5394.
  • Perraud Q, Moynie L, Gasser V, et al. A key role for the periplasmic PfeE esterase in iron acquisition via the siderophore enterobactin in Pseudomonas aeruginosa. ACS Chem Biol. 2018;13(9):2603–2614.
  • Elias S, Degtyar E, Banin E. FvbA is required for vibriobactin utilization in Pseudomonas aeruginosa. Microbiology. 2011;157(Pt 7):2172–2180.
  • Charlang G, Ng B, Horowitz NH, et al. Cellular and extracellular siderophores of Aspergillus nidulans and Penicillium chrysogenum. Mol Cell Biol. 1981;1(2):94–100.
  • Perry RD, Fetherston JD. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect. 2011;13(10):808–817.
  • Chan KG. Exochelin production in Mycobacterium neoaurum. Int J Mol Sci. 2009;10(1):345–353.
  • Lee K, Lee KM, Go J, et al. The ferrichrome receptor A as a new target for Pseudomonas aeruginosa virulence attenuation. FEMS Microbiol Lett. 2016;363(11):fnw104.
  • Arevalo-Ferro C, Hentzer M, Reil G, et al. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ Microbiol. 2003;5(12):1350–1369.
  • Sheldon JR, Laakso HA, Heinrichs DE. Iron acquisition strategies of bacterial pathogens. Microbiol Spectr 4. 2016;4(2):VMBF-0010-2015.
  • Schalk IJ, Guillon L. Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways. Amino Acids. 2013;44(5):1267–1277.
  • Chevalier S, Bouffartigues E, Bazire A, et al. Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. Biochim Biophys Acta Gene Regul Mech. 2019;1862(7):706–721.
  • Llamas MA, Mooij MJ, Sparrius M, et al. Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol. 2008;67(2):458–472.
  • Hunter RC, Asfour F, Dingemans J, et al. Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. mBio 4. 2013;4(4):e00557–13.
  • Lau CK, Krewulak KD, Vogel HJ. Bacterial ferrous iron transport: the Feo system. FEMS Microbiol Rev. 2016;40(2):273–298.
  • Kreamer NN, Wilks JC, Marlow JJ, Coleman ML, et al. BqsR/BqsS constitute a two-component system that senses extracellular Fe(II) in Pseudomonas aeruginosa. J Bacteriol. 2012;194(5):1195–1204.
  • Wang Y, Newman DK. Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ Sci Technol. 2008;42(7):2380–2386.
  • Dong YH, Zhang XF, An SW, et al. A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa. Commun Integr Biol. 2008;1(1):88–96.
  • Reinhart AA, Powell DA, Nguyen AT, et al. The prrF-encoded small regulatory RNAs are required for iron homeostasis and virulence of Pseudomonas aeruginosa. Infect Immun. 2015;83(3):863–875.
  • Vasil ML. How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. Biometals. 2007;20(3–4):587–601.
  • Nelson CE, Huang W, Brewer LK, et al. Proteomic analysis of the Pseudomonas aeruginosa iron starvation response reveals PrrF small regulatory RNA-dependent iron regulation of twitching motility, Amino Acid Metabolism, and Zinc Homeostasis Proteins. J Bacteriol. 2019;201(12):e00754–18.
  • Rasamiravaka T, Labtani Q, Duez P, et al. The formation of biofilms by Pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. Biomed Res Int. 2015;2015:759348.
  • Withers H, Swift S, Williams P. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol. 2001;4(2):186–193.
  • Gooderham WJ, Hancock RE. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev. 2009;33(2):279–294.
  • Goodman AL, Kulasekara B, Rietsch A, et al. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell. 2004;7(5):745–754.
  • Ventre I, Goodman AL, Vallet-Gely I, et al. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA. 2006;103(1):171–176.
  • Colley B, Dederer V, Carnell M, et al. SiaA/D interconnects c-di-GMP and RsmA signaling to coordinate cellular aggregation of Pseudomonas aeruginosa in response to environmental conditions. Front Microbiol. 2016;7:179.
  • Ha DG, 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.
  • Zhu B, Liu C, Liu S, et al. Membrane association of SadC enhances its diguanylate cyclase activity to control exopolysaccharides synthesis and biofilm formation in Pseudomonas aeruginosa. Environ Microbiol. 2016;18(10):3440–3452.
  • Romano AA, Hahn T, Davis N, et al. The Fe(III) and Ga(III) coordination chemistry of 3-(1-hydroxymethylidene) and 3-(1-hydroxydecylidene)-5-(2-hydroxyethyl)pyrrolidine-2,4-dione: novel tetramic acid degradation products of homoserine lactone bacterial quorum sensing molecules. J Inorg Biochem. 2012;107(1):96–103.
  • Bredenbruch F, Geffers R, Nimtz M, et al. The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol. 2006;8(8):1318–1329.
  • Glick R, Gilmour C, Tremblay J, et al. Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol. 2010;192(12):2973–2980.
  • Bollinger N, Hassett DJ, Iglewski BH, et al. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J Bacteriol. 2001;183(6):1990–1996.
  • Djapgne L, Panja S, Brewer LK, et al. The Pseudomonas aeruginosa PrrF1 and PrrF2 small regulatory RNAs promote 2-alkyl-4-quinolone production through redundant regulation of the antR mRNA. J Bacteriol. 2018;200(10):e00704–17.
  • Yu S, Wei Q, Zhao T, et al. A survival strategy for Pseudomonas aeruginosa that uses exopolysaccharides to sequester and store iron to stimulate Psl-dependent biofilm formation. Appl Environ Microbiol. 2016;82(21):6403–6413.
  • Jones CJ, Ryder CR, Mann EE, et al. AmrZ modulates Pseudomonas aeruginosa biofilm architecture by directly repressing transcription of the psl operon. J Bacteriol. 2013;195(8):1637–1644.
  • Ma L, Wang S, Wang D, et al. The roles of biofilm matrix polysaccharide Psl in mucoid Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol. 2012;65(2):377–380.
  • Mishra M, Byrd MS, Sergeant S, et al. Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidative response by limiting complement-mediated opsonization. Cell Microbiol. 2012;14(1):95–106.
  • Visaggio D, Pasqua M, Bonchi C, et al. Cell aggregation promotes pyoverdine-dependent iron uptake and virulence in Pseudomonas aeruginosa. Front Microbiol. 2015;6:902.
  • Yang L, Barken KB, Skindersoe ME, et al. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology. 2007;153(Pt 5):1318–1328.
  • Moreau-Marquis S, Coutermarsh B, Stanton BA. Combination of hypothiocyanite and lactoferrin (ALX-109) enhances the ability of tobramycin and aztreonam to eliminate Pseudomonas aeruginosa biofilms growing on cystic fibrosis airway epithelial cells. J Antimicrob Chemother. 2015;70(1):160–166.
  • Gomme PT, McCann KB, Bertolini J. Transferrin: structure, function and potential therapeutic actions. Drug Discov Today. 2005;10(4):267–273.
  • Oglesby-Sherrouse AG, Djapgne L, Nguyen AT, et al. The complex interplay of iron, biofilm formation, and mucoidy affecting antimicrobial resistance of Pseudomonas aeruginosa. Pathog Dis. 2014;70(3):307–320.
  • Rhee KY, Gardiner DF. Clinical relevance of bacteriostatic versus bactericidal activity in the treatment of gram-positive bacterial infections. Clin Infect Dis. 2004;39(5):755–756.
  • Kohanski MA, Dwyer DJ, Hayete B, et al. A common mechanism of cellular death induced by bactericidal antibiotics. Cell. 2007;130(5):797–810.
  • Minandri F, Bonchi C, Frangipani E, et al. Promises and failures of gallium as an antibacterial agent. Future Microbiol. 2014;9(3):379–397.
  • Kaneko Y, Thoendel M, Olakanmi O, et al. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest. 2007;117(4):877–888.
  • DeLeon K, Balldin F, Watters C, et al. Gallium maltolate treatment eradicates Pseudomonas aeruginosa infection in thermally injured mice. Antimicrob Agents Chemother. 2009;53(4):1331–1337.
  • Bonchi C, Imperi F, Minandri F, et al. Repurposing of gallium-based drugs for antibacterial therapy. Biofactors. 2014;40(3):303–312.
  • Shruti S, Salinas AJ, Lusvardi G, et al. Mesoporous bioactive scaffolds prepared with cerium-, gallium- and zinc-containing glasses. Acta Biomater. 2013;9(1):4836–4844.
  • Lusvardi G, Malavasi G, Menabue L, et al. Gallium-containing phosphosilicate glasses: functionalization and in-vitro bioactivity. Mater Sci Eng C Mater Biol Appl. 2013;33(6):3190–3196.
  • Halwani M, Yebio B, Suntres ZE, et al. Co-encapsulation of gallium with gentamicin in liposomes enhances antimicrobial activity of gentamicin against Pseudomonas aeruginosa. J Antimicrob Chemother. 2008;62(6):1291–1297.
  • Hendricks MR, Lashua LP, Fischer DK, et al. Respiratory syncytial virus infection enhances Pseudomonas aeruginosa biofilm growth through dysregulation of nutritional immunity. Proc Natl Acad Sci Usa. 2016;113(6):1642–1647.
  • Ardehali R, Shi L, Janatova J, et al. The inhibitory activity of serum to prevent bacterial adhesion is mainly due to apo-transferrin. J Biomed Mater Res A. 2003;66(1):21–28.
  • Moreau-Marquis S, O’Toole GA, Stanton BA. Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am J Respir Cell Mol Biol. 2009;41(3):305–313.
  • Aali M, Caldwell A, House K, et al. Iron chelation as novel treatment for lung inflammation in cystic fibrosis. Med Hypotheses. 2017;104:86–88.
  • O'May CY, Sanderson K, Roddam LF, et al. Iron-binding compounds impair Pseudomonas aeruginosa biofilm formation, especially under anaerobic conditions. J Med Microbiol. 2009;58(Pt 6):765–773.
  • Qiao J, Purro M, Liu Z, et al. Terpyridine-micelles for inhibiting bacterial biofilm development. ACS Infect Dis. 2018;4(9):1346–1354.
  • Chiang WC, Nilsson M, Jensen PO, et al. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 2013;57(5):2352–2361.
  • Mislin GL, Schalk IJ. Siderophore-dependent iron uptake systems as gates for antibiotic Trojan horse strategies against Pseudomonas aeruginosa. Metallomics. 2014;6(3):408–420.
  • Miller MJ, Zhu H, Xu Y, et al. Utilization of microbial iron assimilation processes for the development of new antibiotics and inspiration for the design of new anticancer agents. Biometals. 2009;22(1):61–75.
  • Huayhuaz J, Vitorino HA, Campos OS, et al. Desferrioxamine and desferrioxamine-caffeine as carriers of aluminum and gallium to microbes via the Trojan Horse Effect. J Trace Elem Med Biol. 2017;41:16–22.
  • Hurley MN, Camara M, Smyth AR. Novel approaches to the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. Eur Respir J. 2012;40(4):1014–1023.
  • Sethupathy S, Prasath KG, Ananthi S, et al. Proteomic analysis reveals modulation of iron homeostasis and oxidative stress response in Pseudomonas aeruginosa PAO1 by curcumin inhibiting quorum sensing regulated virulence factors and biofilm production. J Proteomics. 2016;145:112–126.
  • Pang Z, Raudonis R, Glick BR, et al. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv. 2019;37(1):177–192.
  • Jeevanandam J, Barhoum A, Chan YS, et al. Review on nanoparticles and nanostructured materials: history, sources, toxicity and regulations. Beilstein J Nanotechnol. 2018;9:1050–1074.
  • Wang L, Hu C, Shao L. The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomedicine. 2017;12:1227–1249.
  • Lee JH, Kim YG, Cho MH, et al. ZnO nanoparticles inhibit Pseudomonas aeruginosa biofilm formation and virulence factor production. Microbiol Res. 2014;169(12):888–896.
  • Singh P, Pandit S, Garnaes J, et al. Green synthesis of gold and silver nanoparticles from Cannabis sativa (industrial hemp) and their capacity for biofilm inhibition. Int J Nanomedicine. 2018;13:3571–3591.
  • Guo J, Gao SH, Lu J, et al. Copper oxide nanoparticles induce lysogenic bacteriophage and metal-resistance genes in Pseudomonas aeruginosa PAO1. ACS Appl Mater Interfaces. 2017;9(27):22298–22307.
  • Rajkumari J, Busi S, Vasu AC, et al. Facile green synthesis of baicalein fabricated gold nanoparticles and their antibiofilm activity against Pseudomonas aeruginosa PAO1. Microb Pathog. 2017;107:261–269.
  • Rajkumari J, Magdalane CM, Siddhardha B, et al. Synthesis of titanium oxide nanoparticles using Aloe barbadensis mill and evaluation of its antibiofilm potential against Pseudomonas aeruginosa PAO1. J Photochem Photobiol B, Biol. 2019;201:111667.
  • Liao S, Zhang Y, Pan X, et al. Antibacterial activity and mechanism of silver nanoparticles against multidrug-resistant Pseudomonas aeruginosa. Int J Nanomedicine. 2019;14:1469–1487.
  • Morones-Ramirez JR, Winkler JA, Spina CS, et al. Silver enhances antibiotic activity against gram-negative bacteria. Sci Transl Med. 2013;5:181–190.
  • Dakal TC, Kumar A, Majumdar RS, et al. Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol. 2016;7:1831.
  • Habash MB, Park AJ, Vis EC, et al. Synergy of silver nanoparticles and aztreonam against Pseudomonas aeruginosa PAO1 biofilms. Antimicrob Agents Chemother. 2014;58(10):5818–5830.
  • Habash MB, Goodyear MC, Park AJ, et al. Potentiation of tobramycin by silver nanoparticles against Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 2017;61(11):e00415–17.
  • Al-Shabib NA, Husain FM, Ahmed F, et al. Low temperature synthesis of superparamagnetic iron oxide (Fe3O4) nanoparticles and their ROS mediated inhibition of biofilm formed by food-associated bacteria. Front Microbiol. 2018;9:2567.
  • Pham D, Khan F, Phan T, et al. Biofilm inhibition, modulation of virulence and motility properties by FeOOH nanoparticle in Pseudomonas aeruginosa. Braz J Microbiol. 2019;50(3):791–805.
  • Trotter CL, McVernon J, Ramsay ME, et al. Optimising the use of conjugate vaccines to prevent disease caused by Haemophilus influenzae type b, Neisseria meningitidis and Streptococcus pneumoniae. Vaccine. 2008;26(35):4434–4445.
  • Alteri CJ, Hagan EC, Sivick KE, et al. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog. 2009;5(9):e1000586.
  • Rashid MI, Naz A, Ali A, et al. Prediction of vaccine candidates against Pseudomonas aeruginosa: an integrated genomics and proteomics approach. Genomics. 2017;109(3–4):274–283.
  • Elhosary MA, Bahey-El-Din M, AbdelBary A, El GN, et al. Immunization with the ferric iron-binding periplasmic protein HitA provides protection against Pseudomonas aeruginosa in the murine infection model. Microb Pathog. 2019;131:181–185.
  • Ferreras JA, Ryu JS, Di Lello F, et al. Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol. 2005;1(1):29–32.

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