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Ferritin and ferrihydrite nanoparticles as iron sources for Pseudomonas aeruginosa

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Abstract

Metabolism of iron derived from insoluble and/or scarce sources is essential for pathogenic and environmental microbes. The ability of Pseudomonas aeruginosa to acquire iron from exogenous ferritin was assessed; ferritin is an iron-concentrating and antioxidant protein complex composed of a catalytic protein and caged ferrihydrite nanomineral synthesized from Fe(II) and O2 or H2O2. Ferritin and free ferrihydrite supported growth of P. aeruginosa with indistinguishable kinetics and final culture densities. The P. aeruginosa PAO1 mutant (ΔpvdDΔpchEF), which is incapable of siderophore production, grew as well as the wild type when ferritin was the iron source. Such data suggest that P. aeruginosa can acquire iron by siderophore-independent mechanisms, including secretion of small-molecule reductant(s). Protease inhibitors abolished the growth of the siderophore-free strain on ferritins, with only a small effect on growth of the wild type; predictably, protease inhibitors had no effect on growth with free ferrihydrite as the iron source. Proteolytic activity was higher with the siderophore-free strain, suggesting that the role of proteases in the degradation of ferritin is particularly important for iron acquisition in the absence of siderophores. The combined results demonstrate the importance of both free ferrihydrite, a natural environmental form of iron and a model for an insoluble form of partly denatured ferritin called hemosiderin, and caged ferritin iron minerals as bacterial iron sources. Ferritin is also revealed as a growth promoter of opportunistic, pathogenic bacteria such a P. aeruginosa in diseased tissues such as the cystic fibrotic lung, where ferritin concentrations are abnormally high.

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References

  1. Frederick RE, Mayfield JA, DuBois JL (2009) Biometals 22:583–593

    Article  PubMed  CAS  Google Scholar 

  2. Nairz M, Schroll A, Sonnweber T, Weiss G (2010) Cell Microbiol 12:1691–1702

    Article  PubMed  CAS  Google Scholar 

  3. Otto BR, Verweijvanvught AMJ, Maclaren DM (1992) Crit Rev Microbiol 18:217–233

    Article  PubMed  CAS  Google Scholar 

  4. Vasil ML, Ochsner UA (1999) Mol Microbiol 34:399–413

    Article  PubMed  CAS  Google Scholar 

  5. Wilks A, Burkhard KA (2007) Nat Prod Rep 24:511–522

    Article  PubMed  CAS  Google Scholar 

  6. Wooldridge KG, Williams PH (1993) FEMS Microbiol Rev 12:325–348

    Article  PubMed  CAS  Google Scholar 

  7. San Martin CD, Garri C, Pizarro F, Walter T, Theil EC, Nunez MT (2008) J Nutr 138:659–666

    PubMed  CAS  Google Scholar 

  8. Kumar V, Hagler HK (1999) Interactive case study companion to Robbins pathologic basis of disease, sixth edition (CD-ROM for Windows & Macintosh, individual). Saunders, Philadelphia

    Google Scholar 

  9. Macedo MF, Cruz E, Lacerda R, Porto G, de Sousa M (2005) Blood Cells Mol Dis 35:319–325

    Article  PubMed  CAS  Google Scholar 

  10. Reid DW, Lam QT, Schneider H, Walters EH (2004) Eur Respir J 24:286–291

    Article  PubMed  CAS  Google Scholar 

  11. Stites SW, Plautz MW, Bailey K, O’Brien-Ladner AR, Wesselius LJ (1999) Am J Resp Crit Care Med 160:796–801

    PubMed  CAS  Google Scholar 

  12. Reid DW, Carroll V, O-May C, Champion A, Kirov SM (2007) Eur Respir J 30(2):286–292

    Article  PubMed  CAS  Google Scholar 

  13. Reid DW, Anderson GJ, Lamont IL (2009) Am J Phys Lung Cell Mol Phys 297:L795–L802

    CAS  Google Scholar 

  14. Stites SW, Walters B, O-Brien-Ladner AR, Bailey K, Wesselius LJ (1998) Chest 114:814–819

    Article  PubMed  CAS  Google Scholar 

  15. Cornell RM, Schwertmann U (2003) The iron oxides: structure, properties, reactions, occurrences, and uses, 2nd edn. Wiley-VCH, Weinheim

    Google Scholar 

  16. Gilbert B, Ono RK, Ching KA, Kim CS (2009) J Colloid Interface Sci 339:285–295

    Article  PubMed  CAS  Google Scholar 

  17. Hochella MF Jr, Lower SK, Maurice PA, Penn RL, Sahai N, Sparks DL, Twining BS (2008) Geochim Cosmochim Acta 72:A382–A383

    Google Scholar 

  18. Tidmarsin GF, Klebba PE, Rosenberg LT (1983) J Inorg Biochem 18:161–168

    Article  Google Scholar 

  19. Ingram JM, Blackwood AC (1970) Adv Appl Microbiol 13:267–282

    Article  CAS  Google Scholar 

  20. Cox CD (1986) Infect Immun 52(1):263–270

    PubMed  CAS  Google Scholar 

  21. Huston WM, Potter AJ, Jennings MP, Rello J, Hauser AR, McEwan AG (2004) J Clin Microbiol 42:2806–2809

    Article  PubMed  CAS  Google Scholar 

  22. Martin LW, Reid DW, Sharples KJ, Lamont IL (2011) Biometals 24(6):1059–1067

    Article  PubMed  CAS  Google Scholar 

  23. Andrews SC (2010) Biochim Biophys Acta Gen Subj 1800:691–705

    Article  CAS  Google Scholar 

  24. Theil EC (2011) Curr Opion Chem Biol 15(2):304–311

    Article  CAS  Google Scholar 

  25. Michel FM, Ehm L, Antao SM, Lee PL, Chupas PJ, Liu G, Strongin DR, Schoonen MA, Phillips BL, Parise JB (2007) Science 316:1726–1729

    Article  PubMed  CAS  Google Scholar 

  26. Michel FM, Barron V, Torrent J, Morales MP, Serna CJ, Boily J, Liu Q, Ambrosini A, Cismasu AC, Brown GE Jr (2010) Proc Natl Acad Sci USA 107:2787–2792

    Article  PubMed  CAS  Google Scholar 

  27. Liu G, Debnath S, Paul KW, Han W, Hausner DB, Hosein H, Michel FM, Parise JB, Sparks DL, Strongin DR (2006) Langmuir 22:9313–9321

    Article  PubMed  CAS  Google Scholar 

  28. Michel FM, Hosein H, Hausner DB, Debnath S, Parise JB, Strongin DR (2010) Biochim Biophys Acta Gen Subj 1800:871–885

    Article  CAS  Google Scholar 

  29. Dehner CA, Barton L, Maurice PA, Dubois JL (2011) Environ Sci Technol 45:977–983

    Article  PubMed  CAS  Google Scholar 

  30. Hersman LE, Huang A, Maurice PA, Forsythe JH (2000) Geomicrobiol J 17(4):261–273

    Article  CAS  Google Scholar 

  31. Salas EC, Berelson WM, Hammond DE, Kampf AR, Nealson KH (2010) Geochim Cosmochim Acta 74:574–583

    Article  PubMed  CAS  Google Scholar 

  32. Barton LE, Grant KE, Kosel T, Quicksall AN, Maurice PA (2011) Environ Sci Technol 45(8):3231–3237

    Article  PubMed  CAS  Google Scholar 

  33. Liu XS, Patterson LD, Miller MJ, Theil EC (2007) J Biol Chem 282(44):31821–31825

    Article  PubMed  CAS  Google Scholar 

  34. Poschet J, Perkett E, Deretic V (2002) Trends Mol Med 8:512–519

    Article  PubMed  CAS  Google Scholar 

  35. Treffry A, Hawkins C, Williams JM, Guest GR, Harrison PM (1996) J Biol Inorg Chem 1:49–60

    Article  CAS  Google Scholar 

  36. Dehner CA, Awaya JD, Maurice PA, DuBois JL (2010) Appl Environ Microbiol 76(7):2041–2048

    Article  PubMed  CAS  Google Scholar 

  37. Schwertmann U, Cornell RM (2000) Iron oxide in the laboratory: preparation and characterization. Wiley-VCH, Weinheim

    Book  Google Scholar 

  38. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP (2005) Nat Methods 2(6):443–448

    Article  PubMed  CAS  Google Scholar 

  39. Miller FD, Hershberger CL (1984) Gene 29:247–250

    Article  PubMed  CAS  Google Scholar 

  40. Stookey LL (1970) Anal Chem 42:779

    Article  CAS  Google Scholar 

  41. Essar DW, Eberly L, Hadero A, Crawford IP (1990) J Bacteriol 172:884–900

    PubMed  CAS  Google Scholar 

  42. Kurachi M (1958) Bull Inst Chem Res Kyoto Univ 36:174–187

    Google Scholar 

  43. Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D (2004) Infect Immun 72(7):4275–4278

    Article  PubMed  CAS  Google Scholar 

  44. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK (2011) J Bacteriol 193(14):3606–3617

    Article  PubMed  CAS  Google Scholar 

  45. Newman DK (2006) Nat Chem Biol 2:71–78

    Article  PubMed  Google Scholar 

  46. Dhungana S, Crumbliss AL (2005) Geomicrobiol J 22:87–98

    Article  CAS  Google Scholar 

  47. Whitby PW, Van Wagoner TM, Springer JM, Morton DJ, Seale TW, Stull TL (2006) J Med Microbiol 55:661–668

    Article  PubMed  CAS  Google Scholar 

  48. Kvitko BH, Goodyear A, Propst AL, Dow SW, Schweizer HR (2012) PLoS Negl Trop Dis 6(6):e1715

    Article  PubMed  CAS  Google Scholar 

  49. Shigematsu T, Fukushima J, Oyama M, Tsuda M, Kawamoto S, Okuda K (2001) Microbiol Immunol 45:579–590

    PubMed  CAS  Google Scholar 

  50. Wilderman PJ, Vasil AI, Johnson Z, Wilson MJ, Cunliffe HE, Lamont IL, Vasil ML (2001) Infect Immun 69:5385–5394

    Article  PubMed  CAS  Google Scholar 

  51. Vartivarian SE, Cowart RE (1999) Arch Biochem Biophys 364:75–82

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Cliff Johnston (Purdue University) performed X-ray diffraction analysis of the ferrihydrite samples. Keshia Koehn and Ewa Dzik (University of Notre Dame) assisted with laboratory experiments. C.D. was partially supported by a Bayer Pre-doctoral Fellowship administered by the Center for Environmental Science & Technology (CEST) at the University of Notre Dame, which also provided use of the ICP-OES and Brunauer–Emmett–Teller adsorption isotherm instruments. Jennifer Szymanowski and William Archer provided assistance with ICP-OES and TEM imaging, respectively; the latter was performed at the Notre Dame Integrated Imaging Facility. Garrett Moraski is thanked for helpful discussions.

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Author notes

  1. Carolyn Dehner

    Present address: Biochemistry Program, Smith College, Northampton, MA, USA

  2. Rabindra K. Behera

    Present address: Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC, USA

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN, 46556, USA

    Carolyn Dehner

  2. Children’s Hospital Oakland Research Institute, Oakland, 94609, USA

    Rabindra K. Behera & Elizabeth C. Theil

  3. Department of Civil and Environmental Engineering and Earth Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA

    Nydia Morales-Soto, Joshua Shrout & Patricia A. Maurice

  4. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA

    Nydia Morales-Soto & Joshua Shrout

  5. Biosciences Division, Center for Infectious Diseases and Biodefense Research, SRI International, 140 Research Drive, Harrisonburg, VA, 22802, USA

    Jennifer L. Dubois

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  1. Carolyn Dehner
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Correspondence to Jennifer L. Dubois.

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Dehner, C., Morales-Soto, N., Behera, R.K. et al. Ferritin and ferrihydrite nanoparticles as iron sources for Pseudomonas aeruginosa . J Biol Inorg Chem 18, 371–381 (2013). https://doi.org/10.1007/s00775-013-0981-9

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  • DOI: https://doi.org/10.1007/s00775-013-0981-9

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