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Following iron speciation in the early stages of magnetite magnetosome biomineralization

  • Emre Firlar (a1), Teresa Perez-Gonzalez (a2), Agata Olszewska (a2), Damien Faivre (a2) and Tanya Prozorov (a3)...

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.

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a) Address all correspondence to this author. e-mail: tprozoro@ameslab.gov

References

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1. Hadfield, D.: Magnetic materials in the third millennium. Mater. Des. 10(5), 222 (1989).
2. Hyeon, T.: Chemical synthesis of magnetic nanoparticles. Chem. Commun. (8), 927934 (2003).
3. Shen, J. and Kirschner, J.: Tailoring magnetism in artificially structured materials: The new frontier. Surf. Sci. 500(1–3), 300 (2002).
4. Siegel, R.W.: 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.
5. Sahoo, Y., Goodarzi, A., Swihart, M.T., Ohulchanskyy, T.Y., Kaur, N., Furlani, E.P., and Prasad, P.N.: Aqueous ferrofluid of magnetite nanoparticles: Fluorescence labeling and magnetophoretic control. J. Phys. Chem. B 109(9), 3879 (2005).
6. Azadmanjiri, J., Hojati-Talemi, P., Simon, G.P., Suzuki, K., and Selomulya, C.: Synthesis and electromagnetic interference shielding properties of iron oxide/polypyrrole nanocomposites. Polym. Eng. Sci. 51(2), 247 (2011).
7. McKenna, K.P., Hofer, F., Gilks, D., Lazarov, V.K., Chen, C., Wang, Z., and Ikuhara, Y.: Atomic-scale structure and properties of highly stable antiphase boundary defects in Fe(3)O(4). Nat. Commun. 5, 5740 (2014).
8. Berdunov, N., Mariotto, G., Balakrishnan, K., Murphy, S., and Shvets, I.V.: Oxide templates for self-assembling arrays of metal nanoclusters. Surf. Sci. 600(21), L287 (2006).
9. Bird, S.M., Galloway, J.M., Rawlings, A.E., Bramble, J.P., and Staniland, S.S.: Taking a hard line with biotemplating: Cobalt-doped magnetite magnetic nanoparticle arrays. Nanoscale 7(16), 7340 (2015).
10. Sun, S., Zeng, H., Robinson, D.B., Raoux, S., Rice, P.M., Wang, S.X., and Li, G.: Monodisperse MFe2O4 (M = Fe, Co, Mn) nanoparticles. J. Am. Chem. Soc. 126, 273 (2004).
11. Gupta, A.K. and Gupta, M.: Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26(18), 3995 (2005).
12. Wang, Y.X., Hussain, S.M., and Krestin, G.P.: Superparamagnetic iron oxide contrast agents: Physicochemical characteristics and applications in MR imaging. Eur. Radiol. 11(11), 2319 (2001).
13. Xu, Z.P., Zeng, Q.H., Lu, G.Q., and Yu, A.B.: Inorganic nanoparticles as carriers for efficient cellular delivery. Chem. Eng. Sci. 61(3), 1027 (2006).
14. Prozorov, T., Bazylinski, D.A., Mallapragada, S.K., and Prozorov, R.: Novel magnetic nanomaterials inspired by magnetotactic bacteria: Topical review. Mater. Sci. Eng., R 74(5), 133 (2013).
15. Bazylinski, D.A. and Frankel, R.B.: Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2(3), 217 (2004).
16. Faivre, D.: Formation of magnetic nanoparticle chains in bacterial sys. MRS Bull. 40(06), 509 (2015).
17. Frankel, R.B.: Inorganic particles produced by microorganisms. MRS Proc. 218, 7779 (1990).
18. Frankel, R.B., Papaefthymiou, G.C., Blakemore, R.P., and O'Brien, W.: Fe3O4 precipitation in magnetotactic bacteria. Biochim. Biophys. Acta, Mol. Cell Res. 763(2), 147 (1983).
19. McKay, C.P., Friedmann, E.I., Frankel, R.B., and Bazylinski, D.A.: Magnetotactic bacteria on Earth and on Mars. Astrobiology 3(2), 263 (2003).
20. Mann, S.: Biomineralization—A new branch of Bioinorganic Chemistry. Chem. Unserer Zeit 20(3), 69 (1986).
21. Lowenstam, H.A. and Weiner, S.: On Biomineralization (Oxford University Press, New York, 1989).
22. Prozorov, T.: Magnetic microbes: Bacterial magnetite biomineralization. Seminars in Cell and Developmental Biology 46, 3643 (2015).
23. Gorby, Y.A., Beveridge, T.J., and Blakemore, R.P.: Characterization of the bacterial magnetosome membrane. J. Bacteriol. 170(2), 834 (1988).
24. Faivre, D. and Godec, T.U.: From bacteria to mollusks: The principles underlying the biomineralization of iron oxide materials. Angew. Chem., Int. Ed. 54(16), 4728 (2015).
25. Arakaki, A., Nakazawa, H., Nemoto, M., Mori, T., and Matsunaga, T.: Formation of magnetite by bacteria and its application. J. R. Soc., Interface 5(26), 977 (2008).
26. Bazylinski, D.A. and Frankel, R.B.: Biologically controlled mineralization in prokaryotes. Rev. Mineral. Geochem. 54, 217 (2003).
27. McKay, D.S., Gibson, E.K., Thomas-Keprta, K.L., Vali, H., Romanek, C.S., Clemett, S.J., Chillier, X.D.F., Maechling, C.R., and Zare, R.N.: Search for past life on Mars: Possible relic biogenic activity in martian meteorite ALH84001. Science 273(5277), 924 (1996).
28. Thomas-Keprta, K.L., Clemett, S.J., Bazylinski, D.A., Kirschvink, J.L., McKay, D.S., Wentworth, S.J., Vali, H., Gibson, E.K., McKay, M.F., and Romanek, C.S.: Truncated hexa-octahedral magnetite crystals in ALH84001: Presumptive biosignatures. Proc. Natl. Acad. Sci. U. S. A. 98(5), 2164 (2001).
29. Hoover, R.B. and Rozanov, A.Y.: Astrobiology: Traces of life in the cosmos. Proc. SPIE-Int. Soc. Opt. Eng. 4765, 1 (2002).
30. Barber, D.J. and Scott, E.R.D.: Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001. Proc. Natl. Acad. Sci. U. S. A. 99(10), 6556 (2002).
31. Bradley, J.P., McSween, H.Y. Jr., and Harvey, R.P.: Epitaxial growth of nanophase magnetite in Martian meteorite Allan Hills 84001: Implications for biogenic mineralization. Meteorit. Planet. Sci. 33(4), 765 (1998).
32. Klem, M.T., Resnick, D.A., Gilmore, K., Young, M., Idzerda Yves, U., and Douglas, T.: 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).
33. Klem, M.T., Young, M., and Douglas, T.: Biomimetic magnetic nanoparticles. Mater. Today 8(9), 28 (2005).
34. Heyen, U. and Schüler, D.: Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl. Microbiol. Biotechnol. 61(5–6), 536 (2003).
35. Rai, M. and Posten, C.: Green Biosynthesis of Nanoparticles: Mechanisms and Applications (CABI, Oxfordshire, 2013).
36. Valverde-Tercedor, C., Montalban-Lopez, M., Perez-Gonzalez, T., Sanchez-Quesada, M.S., Prozorov, T., Pineda-Molina, E., Fernandez-Vivas, M.A., Rodriguez-Navarro, A.B., Trubitsyn, D., Bazylinski, D.A., and Jimenez-Lopez, C.: 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).
37. Arakaki, A., Webb, J., and Matsunaga, T.: A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J. Biol. Chem. 278(10), 8745 (2003).
38. Arakaki, A., Masuda, F., Amemiya, Y., Tanaka, T., and Matsunaga, T.: 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).
39. Galloway, J.M., Bramble, J.P., Rawlings, A.E., Burnell, G., Evans, S.D., and Staniland, S.S.: Biotemplated magnetic nanoparticle arrays. Small 8(2), 204 (2012).
40. Kolinko, I., Lohsse, A., Borg, S., Raschdorf, O., Jogler, C., Tu, Q., Posfai, M., Tompa, E., Plitzko, J.M., Brachmann, A., Wanner, G., Mueller, R., Zhang, Y., and Schueler, D.: Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat. Nanotechnol. 9(3), 193 (2014).
41. Schuler, D.: The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol. 5(4), 209 (2002).
42. Faivre, D., Bottger, L.H., Matzanke, B.F., and Schuler, D.: 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).
43. Staniland, S., Ward, B., Harrison, A., van der Laan, G., and Telling, N.: Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism. Proc. Natl. Acad. Sci. 104(49), 19524 (2007).
44. Baumgartner, J., Morin, G., Menguy, N., Perez Gonzalez, T., Widdrat, M., Cosmidis, J., and Faivre, D.: 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).
45. Colliex, C., Manoubi, T., and Ortiz, C.: Electron-energy-loss-spectroscopy near-edge fine structures in the iron-oxygen system. Phys. Rev. B: Condens. Matter 44(20), 11402 (1991).
46. Tafto, J. and Krivanek, O.L.: Site-specific valence determination by electron energy-loss spectroscopy. Phys. Rev. Lett. 48(8), 560 (1982).
47. Cai, R.S., Li, T., Wang, Y.Q., Wang, C., Yuan, L., and Zhou, G.W.: Formation of modulated structures in single-crystalline hexagonal α-Fe2O3 nanowires. J Nanopart. Res. 14(8), 1 (2012).
48. Gloter, A., Zbinden, M., Guyot, F., Gaill, F., and Colliex, C.: TEM-EELS study of natural ferrihydrite from geological–biological interactions in hydrothermal systems. Earth Planet. Sci. Lett. 222(3–4), 947 (2004).
49. Ochoa, N., Bello, M., Sancristóbal, J., Balsamo, V., Albornoz, A., and Brito, J.L.: Modified cassava starches as potential corrosion inhibitors for sustainable development. Mater. Res. 16, 1209 (2013).
50. Bischoff, J. and Motta, A.T.: EFTEM and EELS analysis of the oxide layer formed on HCM12A exposed to SCW. J. Nucl. Mater. 430(1–3), 171 (2012).
51. Taylor, A.P., Barry, J.C., and Webb, R.I.: Structural and morphological anomalies in magnetosomes: Possible biogenic origin for magnetite in ALH84001. J. Microsc. 201(1), 84 (2001).
52. Fdez-Gubieda, M.L., Muela, A., Alonso, J., Garcia-Prieto, A., Olivi, L., Fernandez-Pacheco, R., and Barandiaran, J.M.: Magnetite biomineralization in Magnetospirillum gryphiswaldense: Time-resolved magnetic and structural studies. ACS Nano 7(4), 3297 (2013).
53. Schüler, D. and Baeuerlein, E.: Iron transport and magnetite crystal formation of the magnetic bacterium Magnetospirillum gryphiswaldense. J. Phys. IV 7, 647 (1997).
54. Grünberg, K., Mueller, E-C., Otto, A., Reszka, R., Linder, D., Kube, M., Reinhardt, R., and Schüler, D.: Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70(2), 1040 (2004).
55. Tanaka, M., Okamura, Y., Arakaki, A., Tanaka, T., Takeyama, H., and Matsunaga, T.: Origin of magnetosome membrane: Proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6(19), 5234 (2006).
56. Mann, S., Webb, J., and Williams, R.J.P. eds.: Biomineralization. Chemical and Biochemical Perspectives (VCH, Weinheim, 1989).
57. Mann, S., Frankel, R.B., and Blakemore, R.P.: Structure, morphology and crystal growth of bacterial magnetite. Nature 310(5976), 405 (1984).
58. Mann, S., Sparks, N.H.C., and Blakemore, R.P.: Structure, morphology and crystal growth of anisotropic magnetite crystals in magnetotactic bacteria. Proc. Roy. Soc. B 231, 477 (1987).
59. Frankel, R.B., Blakemore, R.P., and Wolfe, R.S.: Magnetite in freshwater magnetotactic bacteria. Science (Washington, DC, U. S.) 203(4387), 1355 (1979).
60. Kirschvink, J.L. and Lowenstam, H.A.: Mineralization and magnetization of chiton teeth: Paleomagnetic, sedimentologic, and biologic implications of organic magnetite. Earth Planet. Sci. Lett. 44(2), 193 (1979).
61. Abe, M., Ishihara, T., and Kitamoto, Y.: Magnetite film growth at 30 °C on organic monomolecular layer, mimicking bacterial magnetosome synthesis. J. Appl. Phys. 85(8), 5705 (1999).
62. Pearce, C.I., Henderson, C.M.B., Pattrick, R.A.D., van der Laan, G., and Vaughan, D.J.: 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).
63. Stevens, J.G., Khasanov, A.M., and Mabe, D.R.: Mössbauer and X-ray diffraction investigations of a series of B-doped ferrihydrites. In LACAME 2004, Mercader, R.C., Gancedo, J.R., Cabral Prieto, A., and Baggio-Saitovitch, E., eds (Springer: Berlin, Heidelberg, 2005); p. 83.
64. Swanson, H.E., McMurdie, H.F., Morris, M.C., and Evans, E.H.: Data for 80 substances. In Standard X-ray Diffraction Powder Patterns (US Dept. of Commerce, Springfield, 1967); Section 5.
65. López-Walle, B.C. and Reyes-Melo, E.: Characterization and dynamics of polymer microactuators. In Smart Materials-based Actuators at the Micro/Nano-scale, Rakotondrabe, M., ed. (Springer, New York, 2013); p. 15.
66. Morris, M.C., McMurdie, H.F., Evans, E.H., Paretzkin, B., Parker, H.S., and Panagiotopoulos, N.C.: Data for 58 substances. In Standard X-ray Diffraction Powder Patterns (1976). Section 18.
67. Fischer, A., Schmitz, M., Aichmayer, B., Fratzl, P., and Faivre, D.: Structural purity of magnetite nanoparticles in magnetotactic bacteria. J. R. Soc., Interface 8(60), 1011 (2011).
68. Lagoeiro, L.E.: Transformation of magnetite to hematite and its influence on the dissolution of iron oxide minerals. J. Metamorph. Geol. 16(3), 415 (1998).
69. Kalirai, S.S., Bazylinski, D.A., and Hitchcock, A.P.: Anomalous magnetic orientations of magnetosome chains in a magnetotactic bacterium: Magnetovibrio blakemorei strain MV-1. PLoS One 8(1), e53368 (2013).
70. Faivre, D., Menguy, N., Posfai, M., and Schüler, D.: Environmental parameters affect the physical properties of fast-growing magnetosomes. Am. Mineral. 93(2–3), 463 (2008).
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