Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-18T02:54:10.775Z Has data issue: false hasContentIssue false
  • English
  • Français

Following iron speciation in the early stages of magnetite magnetosome biomineralization

Published online by Cambridge University Press:  26 February 2016

Emre Firlar ,
Teresa Perez-Gonzalez ,
Agata Olszewska ,
Damien Faivre  and
Tanya Prozorov
Emre Firlar
Affiliation:
Emergent Atomic and Magnetic Structures, Division of Materials Sciences and Engineering, US Department of Energy Ames Laboratory, Ames, Iowa 50011, USA
Teresa Perez-Gonzalez
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424 Potsdam, Germany
Agata Olszewska
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424 Potsdam, Germany
Damien Faivre
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm, 14424 Potsdam, Germany
Tanya Prozorov*
Affiliation:
Emergent Atomic and Magnetic Structures, Division of Materials Sciences and Engineering, Ames Laboratory, Ames, Iowa 50011, USA
*
a)Address all correspondence to this author. e-mail: tprozoro@ameslab.gov
Get access

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.

Keywords

nucleation & growthnanoscalecrystallographic structure
Type
Biomineralization and Biomimetics Reviews
Information
Journal of Materials Research , Volume 31 , Issue 5 , 14 March 2016 , pp. 547 - 555
Check for updates
Copyright
Copyright © Materials Research Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Hadfield, D.: Magnetic materials in the third millennium. Mater. Des. 10(5), 222 (1989).CrossRefGoogle Scholar
Hyeon, T.: Chemical synthesis of magnetic nanoparticles. Chem. Commun. (8), 927–934 (2003).CrossRefGoogle ScholarPubMed
Shen, J. and Kirschner, J.: Tailoring magnetism in artificially structured materials: The new frontier. Surf. Sci. 500(1–3), 300 (2002).CrossRefGoogle Scholar
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.Google Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Gupta, A.K. and Gupta, M.: Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26(18), 3995 (2005).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
Bazylinski, D.A. and Frankel, R.B.: Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2(3), 217 (2004).CrossRefGoogle ScholarPubMed
Faivre, D.: Formation of magnetic nanoparticle chains in bacterial sys. MRS Bull. 40(06), 509 (2015).CrossRefGoogle Scholar
Frankel, R.B.: Inorganic particles produced by microorganisms. MRS Proc. 218, 77–79 (1990).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
Mann, S.: Biomineralization—A new branch of Bioinorganic Chemistry. Chem. Unserer Zeit 20(3), 69 (1986).CrossRefGoogle Scholar
Lowenstam, H.A. and Weiner, S.: On Biomineralization (Oxford University Press, New York, 1989).CrossRefGoogle Scholar
Prozorov, T.: Magnetic microbes: Bacterial magnetite biomineralization. Seminars in Cell and Developmental Biology 46, 36–43 (2015).CrossRefGoogle Scholar
Gorby, Y.A., Beveridge, T.J., and Blakemore, R.P.: Characterization of the bacterial magnetosome membrane. J. Bacteriol. 170(2), 834 (1988).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Bazylinski, D.A. and Frankel, R.B.: Biologically controlled mineralization in prokaryotes. Rev. Mineral. Geochem. 54, 217 (2003).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Hoover, R.B. and Rozanov, A.Y.: Astrobiology: Traces of life in the cosmos. Proc. SPIE-Int. Soc. Opt. Eng. 4765, 1 (2002).Google Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Klem, M.T., Young, M., and Douglas, T.: Biomimetic magnetic nanoparticles. Mater. Today 8(9), 28 (2005).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
Rai, M. and Posten, C.: Green Biosynthesis of Nanoparticles: Mechanisms and Applications (CABI, Oxfordshire, 2013).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
Schuler, D.: The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol. 5(4), 209 (2002).Google ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Tafto, J. and Krivanek, O.L.: Site-specific valence determination by electron energy-loss spectroscopy. Phys. Rev. Lett. 48(8), 560 (1982).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Schüler, D. and Baeuerlein, E.: Iron transport and magnetite crystal formation of the magnetic bacterium Magnetospirillum gryphiswaldense. J. Phys. IV 7, 647 (1997).Google Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
Mann, S., Webb, J., and Williams, R.J.P. eds.: Biomineralization. Chemical and Biochemical Perspectives (VCH, Weinheim, 1989).Google Scholar
Mann, S., Frankel, R.B., and Blakemore, R.P.: Structure, morphology and crystal growth of bacterial magnetite. Nature 310(5976), 405 (1984).CrossRefGoogle Scholar
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).Google Scholar
Frankel, R.B., Blakemore, R.P., and Wolfe, R.S.: Magnetite in freshwater magnetotactic bacteria. Science (Washington, DC, U. S.) 203(4387), 1355 (1979).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
Supplementary material: Image

Firlar supplementary material

Figure S1

Download Firlar supplementary material(Image)
Image 36.5 KB
Supplementary material: Image

Firlar supplementary material

Figure S2

Download Firlar supplementary material(Image)
Image 119.1 KB
Supplementary material: Image

Firlar supplementary material

Table S1

Download Firlar supplementary material(Image)
Image 59 KB
Supplementary material: Image

Firlar supplementary material

Table S2

Download Firlar supplementary material(Image)
Image 44.7 KB