Following iron speciation in the early stages of magnetite magnetosome biomineralization

Firlar, Emre; Perez-Gonzalez, Teresa; Olszewska, Agata; Faivre, Damien; Prozorov, Tanya

doi:10.1557/jmr.2016.33

Title: Following iron speciation in the early stages of magnetite magnetosome biomineralization

Journal Article · Fri Feb 26 00:00:00 EST 2016 · Journal of Materials Research

DOI:https://doi.org/10.1557/jmr.2016.33· OSTI ID:1234446

Firlar, Emre ^[1]; Perez-Gonzalez, Teresa ^[2]; Olszewska, Agata ^[2]; Faivre, Damien ^[2]; Prozorov, Tanya ^[1]

Ames Lab., Ames, IA (United States)
Max Planck Institute of Colloids and Interfaces, Potsdam (Germany)

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. Furthermore, 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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Research Organization:: Ames Laboratory (AMES), Ames, IA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-07CH11358

OSTI ID:: 1234446

Report Number(s):: IS-J-8776; applab

Journal Information:: Journal of Materials Research, Vol. 2016, Issue 2; ISSN 0884-2914

Publisher:: Materials Research SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 11 works

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References (65)

Standard x-ray diffraction powder patterns : Morris, Marlene C.; McMurdie, Howard F.; Evans, Eloise H. https://doi.org/10.6028/NBS.MONO.25-13	report	January 1976
Inorganic nanoparticles as carriers for efficient cellular delivery Xu, Zhi Ping; Zeng, Qing Hua; Lu, Gao Qing Chemical Engineering Science, Vol. 61, Issue 3 https://doi.org/10.1016/j.ces.2005.06.019	journal	February 2006
Size control of in vitro synthesized magnetite crystals by the MamC protein of Magnetococcus marinus strain MC-1 Valverde-Tercedor, C.; Montalbán-López, M.; Perez-Gonzalez, T. Applied Microbiology and Biotechnology, Vol. 99, Issue 12 https://doi.org/10.1007/s00253-014-6326-y	journal	January 2015
Characterization and Dynamics of Polymer Microactuators López-Walle, Beatriz Cristina; Reyes-Melo, Edgar Smart Materials-Based Actuators at the Micro/Nano-Scale https://doi.org/10.1007/978-1-4614-6684-0_2	book	January 2013
A Novel Protein Tightly Bound to Bacterial Magnetic Particles in Magnetospirillum magneticum Strain AMB-1 Arakaki, Atsushi; Webb, John; Matsunaga, Tadashi Journal of Biological Chemistry, Vol. 278, Issue 10 https://doi.org/10.1074/jbc.M211729200	journal	December 2002
Standard x-ray diffraction powder patterns Swanson, H. E.; McMurdie, H. F.; Morris, M. C. National Bureau of Standards https://doi.org/10.6028/NBS.MONO.25-5	report	August 1967
Transformation of magnetite to hematite and its influence on the dissolution of iron oxide minerals: TRANSFORMATION OF MAGNETITE TO HEMATITE Lagoeiro, L. E. Journal of Metamorphic Geology, Vol. 16, Issue 3 https://doi.org/10.1111/j.1525-1314.1998.00144.x	journal	May 1998
Anomalous Magnetic Orientations of Magnetosome Chains in a Magnetotactic Bacterium: Magnetovibrio blakemorei Strain MV-1 Kalirai, Samanbir S.; Bazylinski, Dennis A.; Hitchcock, Adam P. PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053368	journal	January 2013
The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense D., Schüler International Microbiology, Vol. 5, Issue 4 https://doi.org/10.1007/s10123-002-0086-8	journal	December 2002
Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging Wang, Yi-Xiang J.; Hussain, Shahid M.; Krestin, Gabriel P. European Radiology, Vol. 11, Issue 11 https://doi.org/10.1007/s003300100908	journal	May 2001
Intracellular Magnetite Biomineralization in Bacteria Proceeds by a Distinct Pathway Involving Membrane-Bound Ferritin and an Iron(II) Species Faivre, Damien; Böttger, Lars H.; Matzanke, Berthold F. Angewandte Chemie International Edition, Vol. 46, Issue 44 https://doi.org/10.1002/anie.200700927	journal	November 2007
Structural purity of magnetite nanoparticles in magnetotactic bacteria Fischer, Anna; Schmitz, Manuel; Aichmayer, Barbara Journal of The Royal Society Interface, Vol. 8, Issue 60 https://doi.org/10.1098/rsif.2010.0576	journal	January 2011
Characterization of the bacterial magnetosome membrane. Gorby, Y. A.; Beveridge, T. J.; Blakemore, R. P. Journal of Bacteriology, Vol. 170, Issue 2 https://doi.org/10.1128/jb.170.2.834-841.1988	journal	January 1988
Formation of magnetite by bacteria and its application Arakaki, Atsushi; Nakazawa, Hidekazu; Nemoto, Michiko Journal of The Royal Society Interface, Vol. 5, Issue 26 https://doi.org/10.1098/rsif.2008.0170	journal	June 2008
Formation of magnetic nanoparticle chains in bacterial systems Faivre, Damien MRS Bulletin, Vol. 40, Issue 6 https://doi.org/10.1557/mrs.2015.99	journal	June 2015
Origin of magnetosome membrane: Proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane Tanaka, Masayoshi; Okamura, Yoshiko; Arakaki, Atsushi PROTEOMICS, Vol. 6, Issue 19 https://doi.org/10.1002/pmic.200500887	journal	October 2006
Synthesis and electromagnetic interference shielding properties of iron oxide/polypyrrole nanocomposites Azadmanjiri, J.; Hojati-Talemi, P.; Simon, G. P. Polymer Engineering & Science, Vol. 51, Issue 2 https://doi.org/10.1002/pen.21813	journal	September 2010
Mineralization and magnetization of chiton teeth: paleomagnetic, sedimentologic, and biologic implications of organic magnetite Kirschvink, J. L.; Lowenstam, H. A. Earth and Planetary Science Letters, Vol. 44, Issue 2 https://doi.org/10.1016/0012-821X(79)90168-7	journal	August 1979
Synthetic Control over Magnetic Moment and Exchange Bias in All-Oxide Materials Encapsulated within a Spherical Protein Cage Klem, Michael T.; Resnick, Damon A.; Gilmore, Keith Journal of the American Chemical Society, Vol. 129, Issue 1 https://doi.org/10.1021/ja0667561	journal	January 2007
Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates Baumgartner, J.; Morin, G.; Menguy, N. Proceedings of the National Academy of Sciences, Vol. 110, Issue 37 https://doi.org/10.1073/pnas.1307119110	journal	August 2013
Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001 Barber, D. J.; Scott, E. R. D. Proceedings of the National Academy of Sciences, Vol. 99, Issue 10 https://doi.org/10.1073/pnas.102045799	journal	May 2002
Magnetite film growth at 30 °C on organic monomolecular layer, mimicking bacterial magnetosome synthesis Abe, M.; Ishihara, T.; Kitamoto, Y. Journal of Applied Physics, Vol. 85, Issue 8 https://doi.org/10.1063/1.370258	journal	April 1999
Magnetic microbes: Bacterial magnetite biomineralization Prozorov, Tanya Seminars in Cell & Developmental Biology, Vol. 46 https://doi.org/10.1016/j.semcdb.2015.09.003	journal	October 2015
Magnetosome formation in prokaryotes Bazylinski, Dennis A.; Frankel, Richard B. Nature Reviews Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nrmicro842	journal	March 2004
Biomimetic magnetic nanoparticles Klem, Michael T.; Young, Mark; Douglas, Trevor Materials Today, Vol. 8, Issue 9 https://doi.org/10.1016/S1369-7021(05)71078-6	journal	September 2005
Magnetic materials in the third millenium Hadfield, D. Materials & Design, Vol. 10, Issue 5 https://doi.org/10.1016/S0261-3069(89)80058-5	journal	September 1989
Magnetite in Freshwater Magnetotactic Bacteria Frankel, R. B.; Blakemore, R. P.; Wolfe, R. S. Science, Vol. 203, Issue 4387 https://doi.org/10.1126/science.203.4387.1355	journal	March 1979
From Bacteria to Mollusks: The Principles Underlying the Biomineralization of Iron Oxide Materials Faivre, Damien; Godec, Tina Ukmar Angewandte Chemie International Edition, Vol. 54, Issue 16 https://doi.org/10.1002/anie.201408900	journal	April 2015
Oxide templates for self-assembling arrays of metal nanoclusters Berdunov, N.; Mariotto, G.; Balakrishnan, K. Surface Science, Vol. 600, Issue 21 https://doi.org/10.1016/j.susc.2006.07.059	journal	November 2006
Aqueous Ferrofluid of Magnetite Nanoparticles: Fluorescence Labeling and Magnetophoretic Control Sahoo, Yudhisthira; Goodarzi, Alireza; Swihart, Mark T. The Journal of Physical Chemistry B, Vol. 109, Issue 9 https://doi.org/10.1021/jp045402y	journal	March 2005
Site-Specific Valence Determination by Electron Energy-Loss Spectroscopy Taftø, J.; Krivanek, O. L. Physical Review Letters, Vol. 48, Issue 8 https://doi.org/10.1103/PhysRevLett.48.560	journal	February 1982
Biomineralisation: Ein neuer Zweig der bioanorganischen Chemie Mann, Stephen Chemie in unserer Zeit, Vol. 20, Issue 3 https://doi.org/10.1002/ciuz.19860200302	journal	June 1986
Epitaxial growth of nanophase magnetite in Martian meteorite Allan Hills 84001: Implications for biogenic mineralization Bradley, J. P.; Mcsween, H. Y.; Harvey, R. P. Meteoritics & Planetary Science, Vol. 33, Issue 4 https://doi.org/10.1111/j.1945-5100.1998.tb01682.x	journal	July 1998
Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications Gupta, Ajay Kumar; Gupta, Mona Biomaterials, Vol. 26, Issue 18 https://doi.org/10.1016/j.biomaterials.2004.10.012	journal	June 2005
Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters Kolinko, Isabel; Lohße, Anna; Borg, Sarah Nature Nanotechnology, Vol. 9, Issue 3 https://doi.org/10.1038/nnano.2014.13	journal	February 2014
Novel magnetic nanomaterials inspired by magnetotactic bacteria: Topical review Prozorov, Tanya; Bazylinski, Dennis A.; Mallapragada, Surya K. Materials Science and Engineering: R: Reports, Vol. 74, Issue 5 https://doi.org/10.1016/j.mser.2013.04.002	journal	May 2013
Tailoring magnetism in artificially structured materials: the new frontier Shen, J.; Kirschner, J. Surface Science, Vol. 500, Issue 1-3 https://doi.org/10.1016/S0039-6028(01)01557-6	journal	March 2002
Taking a hard line with biotemplating: cobalt-doped magnetite magnetic nanoparticle arrays Bird, Scott M.; Galloway, Johanna M.; Rawlings, Andrea E. Nanoscale, Vol. 7, Issue 16 https://doi.org/10.1039/C5NR00651A	journal	January 2015
Search for Past Life on Mars: Possible Relic Biogenic Activity in Martian Meteorite ALH84001 McKay, D. S.; Gibson, E. K.; Thomas-Keprta, K. L. Science, Vol. 273, Issue 5277 https://doi.org/10.1126/science.273.5277.924	journal	August 1996
Direct determination of cation site occupancies in natural ferrite spinels by L2,3 X-ray absorption spectroscopy and X-ray magnetic circular dichroism Pearce, C. I. American Mineralogist, Vol. 91, Issue 5-6 https://doi.org/10.2138/am.2006.2048	journal	May 2006
Fe3O4 precipitation in magnetotactic bacteria Frankel, Richard B.; Papaefthymiou, Georgia C.; Blakemore, Richard P. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 763, Issue 2 https://doi.org/10.1016/0167-4889(83)90038-1	journal	September 1983
Environmental parameters affect the physical properties of fast-growing magnetosomes Faivre, D.; Menguy, N.; Posfai, M. American Mineralogist, Vol. 93, Issue 2-3 https://doi.org/10.2138/am.2008.2678	journal	February 2008
Atomic-scale structure and properties of highly stable antiphase boundary defects in Fe3O4 McKenna, Keith P.; Hofer, Florian; Gilks, Daniel Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6740	journal	December 2014
Mössbauer and X-Ray Diffraction Investigations of a Series of B-Doped Ferrihydrites Stevens, John G.; Khasanov, Airat M.; Mabe, David R. LACAME 2004 https://doi.org/10.1007/3-540-28960-7_9	book	January 2005
Inorganic Particles Produced by Microorganisms Frankel, Richard B. MRS Proceedings, Vol. 218 https://doi.org/10.1557/PROC-218-77	journal	January 1990
Structural and morphological anomalies in magnetosomes: possible biogenic origin for magnetite in ALH84001 Taylor, A. P.; Barry, J. C.; Webb, R. I. Journal of Microscopy, Vol. 201, Issue 1 https://doi.org/10.1046/j.1365-2818.2001.00760.x	journal	January 2001
Biotemplated Magnetic Nanoparticle Arrays Galloway, Johanna M.; Bramble, Jonathan P.; Rawlings, Andrea E. Small, Vol. 8, Issue 2 https://doi.org/10.1002/smll.201101627	journal	November 2011
Modified cassava starches as potential corrosion inhibitors for sustainable development Ochoa, Nathalie; Bello, Marisela; Sancristóbal, Janet Materials Research, Vol. 16, Issue 6 https://doi.org/10.1590/S1516-14392013005000126	journal	August 2013
Magnetotactic Bacteria on Earth and on Mars McKay, Christopher P.; Friedmann, E. Imre; Frankel, Richard B. Astrobiology, Vol. 3, Issue 2 https://doi.org/10.1089/153110703769016361	journal	June 2003
Electron-energy-loss-spectroscopy near-edge fine structures in the iron-oxygen system Colliex, C.; Manoubi, T.; Ortiz, C. Physical Review B, Vol. 44, Issue 20 https://doi.org/10.1103/PhysRevB.44.11402	journal	November 1991
Structure, morphology and crystal growth of anisotropic magnetite crystals in magnetotactic bacteria Mann, Stephen; Sparks, N. H. C.; Blakemore, R. P. Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 231, Issue 1265, p. 477-487 https://doi.org/10.1098/rspb.1987.0056	journal	September 1987
Magnetite Biomineralization in Magnetospirillum gryphiswaldense : Time-Resolved Magnetic and Structural Studies Fdez-Gubieda, M. Luisa; Muela, Alicia; Alonso, Javier ACS Nano, Vol. 7, Issue 4 https://doi.org/10.1021/nn3059983	journal	April 2013
Biologically Controlled Mineralization in Prokaryotes Bazylinski, D. A. Reviews in Mineralogy and Geochemistry, Vol. 54, Issue 1 https://doi.org/10.2113/0540217	journal	January 2003
Truncated hexa-octahedral magnetite crystals in ALH84001: Presumptive biosignatures Thomas-Keprta, K. L.; Clemett, S. J.; Bazylinski, D. A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 5 https://doi.org/10.1073/pnas.051500898	journal	February 2001
Structure, morphology and crystal growth of bacterial magnetite Mann, Stephen; Frankel, Richard B.; Blakemore, Richard P. Nature, Vol. 310, Issue 5976 https://doi.org/10.1038/310405a0	journal	August 1984
Green biosynthesis of nanoparticles: mechanisms and applications Rai, M.; Posten, C. https://doi.org/10.1079/9781780642239.0000	book	January 2013
Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor Heyen, U.; Schüler, D. Applied Microbiology and Biotechnology, Vol. 61, Issue 5-6 https://doi.org/10.1007/s00253-002-1219-x	journal	February 2003
EFTEM and EELS analysis of the oxide layer formed on HCM12A exposed to SCW Bischoff, Jeremy; Motta, Arthur T. Journal of Nuclear Materials, Vol. 430, Issue 1-3 https://doi.org/10.1016/j.jnucmat.2012.06.017	journal	November 2012
Biochemical and Proteomic Analysis of the Magnetosome Membrane in Magnetospirillum gryphiswaldense Grunberg, K.; Muller, E. -C.; Otto, A. Applied and Environmental Microbiology, Vol. 70, Issue 2 https://doi.org/10.1128/AEM.70.2.1040-1050.2004	journal	February 2004
Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism Staniland, S.; Ward, B.; Harrison, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 49 https://doi.org/10.1073/pnas.0704879104	journal	November 2007
Formation of modulated structures in single-crystalline hexagonal α-Fe2O3 nanowires Cai, R. S.; Li, T.; Wang, Y. Q. Journal of Nanoparticle Research, Vol. 14, Issue 8 https://doi.org/10.1007/s11051-012-1073-4	journal	August 2012
Monodisperse MFe ₂ O ₄ (M = Fe, Co, Mn) Nanoparticles Sun, Shouheng; Zeng, Hao; Robinson, David B. Journal of the American Chemical Society, Vol. 126, Issue 1 https://doi.org/10.1021/ja0380852	journal	January 2004
Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from magnetotactic bacteria Arakaki, Atsushi; Masuda, Fukashi; Amemiya, Yosuke Journal of Colloid and Interface Science, Vol. 343, Issue 1 https://doi.org/10.1016/j.jcis.2009.11.043	journal	March 2010
TEM-EELS study of natural ferrihydrite from geological–biological interactions in hydrothermal systems Gloter, A.; Zbinden, M.; Guyot, F. Earth and Planetary Science Letters, Vol. 222, Issue 3-4 https://doi.org/10.1016/j.epsl.2004.03.040	journal	June 2004
Chemical synthesis of magnetic nanoparticles Hyeon, Taeghwan Chemical Communications, Issue 8 https://doi.org/10.1039/b207789b	journal	December 2002

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