Skip to main content
SpringerLink
Log in

Following iron speciation in the early stages of magnetite magnetosome biomineralization

  • Biomineralization and Biomimetics Reviews
  • Published:
Journal of Materials Research Aims and scope Submit manuscript

Abstract

Understanding magnetosome magnetite biomineralization is of fundamental interest to devising the strategies for bioinspired synthesis of magnetic materials at the nanoscale. Thus, we investigated the early stages of magnetosome formation in this work and correlated the size and emergent crystallinity of magnetosome nanoparticles with the changes in chemical environment of iron and oxygen by utilizing advanced analytical electron microscopy techniques. We observed that magnetosomes in the early stages of biomineralization with the sizes of 5–10 nm were amorphous, with a majority of iron present as Fe3+, indicative of ferric hydroxide. The magnetosomes with intermediate sizes showed partially crystalline structure with a majority of iron present as Fe3+ and trace amounts of Fe2+. The fully maturated magnetosomes were indexed to magnetite. Our approach provides spatially resolved structural and chemical information of individual magnetosomes with different particle sizes, attributed to magnetosomes at different stages of biomineralization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5

Similar content being viewed by others

References

  1. D. Hadfield: Magnetic materials in the third millennium. Mater. Des. 10 (5), 222 (1989).

    CAS  Google Scholar 

  2. T. Hyeon: Chemical synthesis of magnetic nanoparticles. Chem. Commun. (8), 927–934 (2003).

    Google Scholar 

  3. J. Shen and J. Kirschner: Tailoring magnetism in artificially structured materials: The new frontier. Surf. Sci. 500 (1–3), 300 (2002).

    CAS  Google Scholar 

  4. R.W. Siegel: Synthesis, structure and properties of nanostructured materials. In Fundamental Properties of Nanostructured Materials, National School of the Condensed Matter Group, Rimini, Italy, September 20–25, 1993, 1994; p. 3.

    Google Scholar 

  5. Y. Sahoo, A. Goodarzi, M.T. Swihart, T.Y. Ohulchanskyy, N. Kaur, E.P. Furlani, and P.N. Prasad: Aqueous ferrofluid of magnetite nanoparticles: Fluorescence labeling and magnetophoretic control. J. Phys. Chem. B 109 (9), 3879 (2005).

    CAS  Google Scholar 

  6. J. Azadmanjiri, P. Hojati-Talemi, G.P. Simon, K. Suzuki, and C. Selomulya: Synthesis and electromagnetic interference shielding properties of iron oxide/polypyrrole nanocomposites. Polym. Eng. Sci. 51 (2), 247 (2011).

    CAS  Google Scholar 

  7. K.P. McKenna, F. Hofer, D. Gilks, V.K. Lazarov, C. Chen, Z. Wang, and Y. Ikuhara: Atomic-scale structure and properties of highly stable antiphase boundary defects in Fe(3)O(4). Nat. Commun. 5, 5740 (2014).

    CAS  Google Scholar 

  8. N. Berdunov, G. Mariotto, K. Balakrishnan, S. Murphy, and I.V. Shvets: Oxide templates for self-assembling arrays of metal nanoclusters. Surf. Sci. 600 (21), L287 (2006).

    CAS  Google Scholar 

  9. S.M. Bird, J.M. Galloway, A.E. Rawlings, J.P. Bramble, and S.S. Staniland: Taking a hard line with biotemplating: Cobalt-doped magnetite magnetic nanoparticle arrays. Nanoscale 7 (16), 7340 (2015).

    CAS  Google Scholar 

  10. S. Sun, H. Zeng, D.B. Robinson, S. Raoux, P.M. Rice, S.X. Wang, and G. Li: Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. J. Am. Chem. Soc. 126, 273 (2004).

    CAS  Google Scholar 

  11. A.K. Gupta and M. Gupta: Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26 (18), 3995 (2005).

    CAS  Google Scholar 

  12. Y.X. Wang, S.M. Hussain, and G.P. Krestin: Superparamagnetic iron oxide contrast agents: Physicochemical characteristics and applications in MR imaging. Eur. Radiol. 11 (11), 2319 (2001).

    CAS  Google Scholar 

  13. Z.P. Xu, Q.H. Zeng, G.Q. Lu, and A.B. Yu: Inorganic nanoparticles as carriers for efficient cellular delivery. Chem. Eng. Sci. 61 (3), 1027 (2006).

    CAS  Google Scholar 

  14. T. Prozorov, D.A. Bazylinski, S.K. Mallapragada, and R. Prozorov: Novel magnetic nanomaterials inspired by magnetotactic bacteria: Topical review. Mater. Sci. Eng., R 74 (5), 133 (2013).

    Google Scholar 

  15. D.A. Bazylinski and R.B. Frankel: Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2 (3), 217 (2004).

    CAS  Google Scholar 

  16. D. Faivre: Formation of magnetic nanoparticle chains in bacterial sys. MRS Bull. 40 (06), 509 (2015).

    CAS  Google Scholar 

  17. R.B. Frankel: Inorganic particles produced by microorganisms. MRS Proc. 218, 77–79 (1990).

    Google Scholar 

  18. R.B. Frankel, G.C. Papaefthymiou, R.P. Blakemore, and W. O’Brien: Fe3O4 precipitation in magnetotactic bacteria. Biochim. Biophys. Acta, Mol. Cell Res. 763 (2), 147 (1983).

    CAS  Google Scholar 

  19. C.P. McKay, E.I. Friedmann, R.B. Frankel, and D.A. Bazylinski: Magnetotactic bacteria on Earth and on Mars. Astrobiology 3 (2), 263 (2003).

    CAS  Google Scholar 

  20. S. Mann: Biomineralization—A new branch of Bioinorganic Chemistry. Chem. Unserer Zeit 20 (3), 69 (1986).

    CAS  Google Scholar 

  21. H.A. Lowenstam and S. Weiner: On Biomineralization (Oxford University Press, New York, 1989).

    Google Scholar 

  22. T. Prozorov: Magnetic microbes: Bacterial magnetite biomineralization. Seminars in Cell and Developmental Biology 46, 36–43 (2015).

    CAS  Google Scholar 

  23. Y.A. Gorby, T.J. Beveridge, and R.P. Blakemore: Characterization of the bacterial magnetosome membrane. J. Bacteriol. 170 (2), 834 (1988).

    CAS  Google Scholar 

  24. D. Faivre and T.U. Godec: From bacteria to mollusks: The principles underlying the biomineralization of iron oxide materials. Angew. Chem., Int. Ed. 54 (16), 4728 (2015).

    CAS  Google Scholar 

  25. A. Arakaki, H. Nakazawa, M. Nemoto, T. Mori, and T. Matsunaga: Formation of magnetite by bacteria and its application. J. R. Soc., Interface 5 (26), 977 (2008).

    CAS  Google Scholar 

  26. D.A. Bazylinski and R.B. Frankel: Biologically controlled mineralization in prokaryotes. Rev. Mineral. Geochem. 54, 217 (2003).

    CAS  Google Scholar 

  27. D.S. McKay, E.K. Gibson, K.L. Thomas-Keprta, H. Vali, C.S. Romanek, S.J. Clemett, X.D.F. Chillier, C.R. Maechling, and R.N. Zare: Search for past life on Mars: Possible relic biogenic activity in martian meteorite ALH84001. Science 273 (5277), 924 (1996).

    CAS  Google Scholar 

  28. K.L. Thomas-Keprta, S.J. Clemett, D.A. Bazylinski, J.L. Kirschvink, D.S. McKay, S.J. Wentworth, H. Vali, E.K. Gibson, M.F. McKay, and C.S. Romanek: Truncated hexa-octahedral magnetite crystals in ALH84001: Presumptive biosignatures. Proc. Natl. Acad. Sci. U. S. A. 98 (5), 2164 (2001).

    CAS  Google Scholar 

  29. R.B. Hoover and A.Y. Rozanov: Astrobiology: Traces of life in the cosmos. Proc. SPIE-Int. Soc. Opt. Eng. 4765, 1 (2002).

    CAS  Google Scholar 

  30. D.J. Barber and E.R.D. Scott: Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001. Proc. Natl. Acad. Sci. U. S. A. 99 (10), 6556 (2002).

    CAS  Google Scholar 

  31. J.P. Bradley, H.Y. McSween, Jr., and R.P. Harvey: Epitaxial growth of nanophase magnetite in Martian meteorite Allan Hills 84001: Implications for biogenic mineralization. Meteorit. Planet. Sci. 33 (4), 765 (1998).

    CAS  Google Scholar 

  32. M.T. Klem, D.A. Resnick, K. Gilmore, M. Young, U. Idzerda Yves, and T. Douglas: Synthetic control over magnetic moment and exchange bias in all-oxide materials encapsulated within a spherical protein cage. J. Am. Chem. Soc. 129 (1), 197 (2007).

    CAS  Google Scholar 

  33. M.T. Klem, M. Young, and T. Douglas: Biomimetic magnetic nanoparticles. Mater. Today 8 (9), 28 (2005).

    CAS  Google Scholar 

  34. U. Heyen and D. Schüler: Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl. Microbiol. Biotechnol. 61 (5–6), 536 (2003).

    CAS  Google Scholar 

  35. M. Rai and C. Posten: Green Biosynthesis of Nanoparticles: Mechanisms and Applications (CABI, Oxfordshire, 2013).

    Google Scholar 

  36. C. Valverde-Tercedor, M. Montalban-Lopez, T. Perez-Gonzalez, M.S. Sanchez-Quesada, T. Prozorov, E. Pineda-Molina, M.A. Fernandez-Vivas, A.B. Rodriguez-Navarro, D. Trubitsyn, D.A. Bazylinski, and C. Jimenez-Lopez: Size control of in vitro synthesized magnetite crystals by the MamC protein of Magnetococcus marinus strain MC-1. Appl. Microbiol. Biotechnol. 99 (12), 5109 (2015).

    CAS  Google Scholar 

  37. A. Arakaki, J. Webb, and T. Matsunaga: A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J. Biol. Chem. 278 (10), 8745 (2003).

    CAS  Google Scholar 

  38. A. Arakaki, F. Masuda, Y. Amemiya, T. Tanaka, and T. Matsunaga: Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from Magnetotactic bacteria. J. Interface Sci. 343 (1), 65 (2010).

    CAS  Google Scholar 

  39. J.M. Galloway, J.P. Bramble, A.E. Rawlings, G. Burnell, S.D. Evans, and S.S. Staniland: Biotemplated magnetic nanoparticle arrays. Small 8 (2), 204 (2012).

    CAS  Google Scholar 

  40. I. Kolinko, A. Lohsse, S. Borg, O. Raschdorf, C. Jogler, Q. Tu, M. Posfai, E. Tompa, J.M. Plitzko, A. Brachmann, G. Wanner, R. Mueller, Y. Zhang, and D. Schueler: Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat. Nanotechnol. 9 (3), 193 (2014).

    CAS  Google Scholar 

  41. D. Schuler: The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol. 5 (4), 209 (2002).

    CAS  Google Scholar 

  42. D. Faivre, L.H. Bottger, B.F. Matzanke, and D. Schuler: Intracellular magnetite biomineralization in bacteria proceeds by a distinct pathway involving membrane-bound ferritin and an iron(II) species. Angew. Chem., Int. Ed. Engl. 46 (44), 8495 (2007).

    CAS  Google Scholar 

  43. S. Staniland, B. Ward, A. Harrison, G. van der Laan, and N. Telling: Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism. Proc. Natl. Acad. Sci. 104 (49), 19524 (2007).

    CAS  Google Scholar 

  44. J. Baumgartner, G. Morin, N. Menguy, T. Perez Gonzalez, M. Widdrat, J. Cosmidis, and D. Faivre: Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates. Proc. Natl. Acad. Sci. U. S. A. 110 (37), 14883 (2013).

    CAS  Google Scholar 

  45. C. Colliex, T. Manoubi, and C. Ortiz: Electron-energy-loss-spectroscopy near-edge fine structures in the iron-oxygen system. Phys. Rev. B: Condens. Matter 44 (20), 11402 (1991).

    CAS  Google Scholar 

  46. J. Tafto and O.L. Krivanek: Site-specific valence determination by electron energy-loss spectroscopy. Phys. Rev. Lett. 48 (8), 560 (1982).

    CAS  Google Scholar 

  47. R.S. Cai, T. Li, Y.Q. Wang, C. Wang, L. Yuan, and G.W. Zhou: Formation of modulated structures in single-crystalline hexagonal α-Fe2O3 nanowires. J Nanopart. Res. 14 (8), 1 (2012).

    CAS  Google Scholar 

  48. A. Gloter, M. Zbinden, F. Guyot, F. Gaill, and C. Colliex: TEM-EELS study of natural ferrihydrite from geological–biological interactions in hydrothermal systems. Earth Planet. Sci. Lett. 222 (3–4), 947 (2004).

    CAS  Google Scholar 

  49. N. Ochoa, M. Bello, J. Sancristóbal, V. Balsamo, A. Albornoz, and J.L. Brito: Modified cassava starches as potential corrosion inhibitors for sustainable development. Mater. Res. 16, 1209 (2013).

    CAS  Google Scholar 

  50. J. Bischoff and A.T. Motta: EFTEM and EELS analysis of the oxide layer formed on HCM12A exposed to SCW. J. Nucl. Mater. 430 (1–3), 171 (2012).

    CAS  Google Scholar 

  51. A.P. Taylor, J.C. Barry, and R.I. Webb: Structural and morphological anomalies in magnetosomes: Possible biogenic origin for magnetite in ALH84001. J. Microsc. 201 (1), 84 (2001).

    CAS  Google Scholar 

  52. M.L. Fdez-Gubieda, A. Muela, J. Alonso, A. Garcia-Prieto, L. Olivi, R. Fernandez-Pacheco, and J.M. Barandiaran: Magnetite biomineralization in Magnetospirillum gryphiswaldense: Time-resolved magnetic and structural studies. ACS Nano 7 (4), 3297 (2013).

    CAS  Google Scholar 

  53. D. Schüler and E. Baeuerlein: Iron transport and magnetite crystal formation of the magnetic bacterium Magnetospirillum gryphiswaldense. J. Phys. IV 7, 647 (1997).

    Google Scholar 

  54. K. Grünberg, E-C. Mueller, A. Otto, R. Reszka, D. Linder, M. Kube, R. Reinhardt, and D. Schüler: Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70 (2), 1040 (2004).

    Google Scholar 

  55. M. Tanaka, Y. Okamura, A. Arakaki, T. Tanaka, H. Takeyama, and T. Matsunaga: Origin of magnetosome membrane: Proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6 (19), 5234 (2006).

    CAS  Google Scholar 

  56. S. Mann, J. Webb, and R.J.P. Williams eds.: Biomineralization. Chemical and Biochemical Perspectives (VCH, Weinheim, 1989).

    Google Scholar 

  57. S. Mann, R.B. Frankel, and R.P. Blakemore: Structure, morphology and crystal growth of bacterial magnetite. Nature 310 (5976), 405 (1984).

    Google Scholar 

  58. S. Mann, N.H.C. Sparks, and R.P. Blakemore: Structure, morphology and crystal growth of anisotropic magnetite crystals in magnetotactic bacteria. Proc. Roy. Soc. B 231, 477 (1987).

    CAS  Google Scholar 

  59. R.B. Frankel, R.P. Blakemore, and R.S. Wolfe: Magnetite in freshwater magnetotactic bacteria. Science (Washington, DC, U. S.) 203 (4387), 1355 (1979).

    CAS  Google Scholar 

  60. J.L. Kirschvink and H.A. Lowenstam: Mineralization and magnetization of chiton teeth: Paleomagnetic, sedimentologic, and biologic implications of organic magnetite. Earth Planet. Sci. Lett. 44 (2), 193 (1979).

    Google Scholar 

  61. M. Abe, T. Ishihara, and Y. Kitamoto: Magnetite film growth at 30 °C on organic monomolecular layer, mimicking bacterial magnetosome synthesis. J. Appl. Phys. 85 (8), 5705 (1999).

    CAS  Google Scholar 

  62. C.I. Pearce, C.M.B. Henderson, R.A.D. Pattrick, G. van der Laan, and D.J. Vaughan: Direct determination of cation site occupancies in natural ferrite spinels by L2,3 X-ray absorption spectroscopy and X-ray magnetic circular dichroism. Am. Mineral. 91 (5–6), 880 (2006).

    CAS  Google Scholar 

  63. J.G. Stevens, A.M. Khasanov, and D.R. Mabe: Mössbauer and X-ray diffraction investigations of a series of B-doped ferrihydrites. In LACAME 2004, R.C. Mercader, J.R. Gancedo, A. Cabral Prieto, and E. Baggio-Saitovitch, eds (Springer: Berlin, Heidelberg, 2005); p. 83.

    Google Scholar 

  64. H.E. Swanson, H.F. McMurdie, M.C. Morris, and E.H. Evans: Data for 80 substances. In Standard X-ray Diffraction Powder Patterns (US Dept. of Commerce, Springfield, 1967); Section 5.

    Google Scholar 

  65. B.C. López-Walle and E. Reyes-Melo: Characterization and dynamics of polymer microactuators. In Smart Materials-based Actuators at the Micro/Nano-scale, M. Rakotondrabe, ed. (Springer, New York, 2013); p. 15.

    Google Scholar 

  66. M.C. Morris, H.F. McMurdie, E.H. Evans, B. Paretzkin, H.S. Parker, and N.C. Panagiotopoulos: Data for 58 substances. In Standard X-ray Diffraction Powder Patterns (1976). Section 18.

  67. A. Fischer, M. Schmitz, B. Aichmayer, P. Fratzl, and D. Faivre: Structural purity of magnetite nanoparticles in magnetotactic bacteria. J. R. Soc., Interface 8 (60), 1011 (2011).

    CAS  Google Scholar 

  68. L.E. Lagoeiro: Transformation of magnetite to hematite and its influence on the dissolution of iron oxide minerals. J. Metamorph. Geol. 16 (3), 415 (1998).

    CAS  Google Scholar 

  69. S.S. Kalirai, D.A. Bazylinski, and A.P. Hitchcock: Anomalous magnetic orientations of magnetosome chains in a magnetotactic bacterium: Magnetovibrio blakemorei strain MV-1. PLoS One 8 (1), e53368 (2013).

    CAS  Google Scholar 

  70. D. Faivre, N. Menguy, M. Posfai, and D. Schüler: Environmental parameters affect the physical properties of fast-growing magnetosomes. Am. Mineral. 93 (2–3), 463 (2008).

    CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

This work was supported by the U.S. Department of Energy (DOE), Office of Science, Basic Energy Sciences, Division of Materials Sciences and Engineering. T.P. acknowledges support from the Department of Energy Office of Science Early Career Research Award, Biomolecular Materials Program. The research was performed at the Ames Laboratory, which is operated for the U.S. Department of Energy by Iowa State University under Contract No. DE-AC02-07CH11358. D.F. acknowledges financial support from the Max Planck Society and the European Research Council (Starting Grant MB2 No. 256915).

Author information

Authors and Affiliations

  1. Emergent Atomic and Magnetic Structures, Division of Materials Sciences and Engineering, US Department of Energy Ames Laboratory, Ames, Iowa, 50011, USA

    Emre Firlar & Tanya Prozorov

  2. Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424, Potsdam, Germany

    Teresa Perez-Gonzalez, Agata Olszewska & Damien Faivre

Authors
  1. Emre Firlar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teresa Perez-Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agata Olszewska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Damien Faivre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tanya Prozorov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tanya Prozorov.

Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Firlar, E., Perez-Gonzalez, T., Olszewska, A. et al. Following iron speciation in the early stages of magnetite magnetosome biomineralization. Journal of Materials Research 31, 547–555 (2016). https://doi.org/10.1557/jmr.2016.33

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/jmr.2016.33

Search

Navigation