Cited by 20Geomagnetism and Paleomagnetism StudiesMagnetic Properties and Synthesis of FerritesMicrobial Fuel Cells and Bioremediation

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Localized iron accumulation precedes nucleation and growth of magnetite crystals in magnetotactic bacteria

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Abstract

Many magnetotactic bacteria (MTB) biomineralize magnetite crystals that nucleate and grow inside intracellular membranous vesicles that originate from invaginations of the cytoplasmic membrane. The crystals together with their surrounding membranes are referred to magnetosomes. Magnetosome magnetite crystals nucleate and grow using iron transported inside the vesicle by specific proteins. Here we address the question: can iron transported inside MTB for the production of magnetite crystals be spatially mapped using electron microscopy? Cultured and uncultured MTB from brackish and freshwater lagoons were studied using analytical transmission electron microscopy in an attempt to answer this question. Scanning transmission electron microscopy was used at sub-nanometric resolution to determine the distribution of elements by implementing high sensitivity energy dispersive X-ray (EDS) mapping and electron energy loss spectroscopy (EELS). EDS mapping showed that magnetosomes are enmeshed in a magnetosomal matrix in which iron accumulates close to the magnetosome forming a continuous layer visually appearing as a corona. EELS, obtained at high spatial resolution, confirmed that iron was present close to and inside the lipid bilayer magnetosome membrane. This study provides important clues to magnetite formation in MTB through the discovery of a mechanism where iron ions accumulate prior to magnetite biomineralization.

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Research works printed but not linked: 40

  1. Cappellen, P. V. Biomineralization and global biogeochemical cycles. Rev. in Mineral. Geochem. 54, 357–381 (2003). · DOI
  2. Bazylinski, D. A. & Frankel, R. B. Magnetosome formation in prokaryotes. Nature Rev. Microbiol. 2, 217–230 (2004). · DOI
  3. Frankel, R. B., Bazylinski, D. A., Johnson, M. S. & Taylor, B. L. Magneto-aerotaxis in marine coccoid bacteria. Biophys. J. 73, 994–1000 (1997). · DOI
  4. Lowenstam, H. A. Minerals formed by organisms. Science 211, 1126–1131 (1981). · DOI · Paper page
  5. Pósfai, M., Lefèvre, C. T., Trubitsyn, D., Bazylinski, D. A. & Frankel, R. B. Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front. Microbiol. 4, 344, doi:10.3389/fmicb.2013.00344 (2013). · DOI
  6. Rahn-Lee, L. et al. A genetic strategy for probing the functional diversity of magnetosome formation. PLoS Genet. 11, e1004811, doi:10.1371/journal.pgen.1004811 (2015). · DOI
  7. Cornejo, E., Subramanian, P., Li, Z., Jensen, G. J. & Komeili, A. Dynamic remodeling of the magnetosome membrane is triggered by the initiation of biomineralization. MBio. 7, e01898–15, doi:10.1128/mBio.01898-15 (2016). · DOI
  8. Nudelman, H. et al. Structure-function studies of the magnetite-biomineralizing magnetosome-associated protein MamC. J. Struct. Biol. 194, 244–252 (2016). · DOI
  9. Yamagishi, A. et al. Control of magnetite nanocrystal morphology in magnetotactic bacteria by regulation of mms7 gene expression. Sci. Rep. 6, 29785, doi:10.1038/srep29785 (2016). · DOI
  10. Uebe, R. & Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nature Rev. Microbiol. 14, 621–637 (2016). · DOI
  11. Grünberg, K., Wawer, C., Tebo, B. M. & Schüler, D. A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Appl. Environ. Microbiol. 67, 4573–4582 (2001). · DOI
  12. Ullrich, S., Kube, M., Schübbe, S., Reinhardt, R. & Schüler, D. A hypervariable 130kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J. Bacteriol. 187, 7176–7184 (2005). · DOI
  13. Faivre, D. & Godec, U. K. From bacteria to mollusks: the principles underlying the biomineralization of iron oxide materials. Angew. Chem. Int. Ed. Engl. 54, 4728–4747 (2015). · DOI
  14. Mandernack, K. W., Bazylinski, D. A., Shanks, W. C. & Bullen, T. D. Oxygen and iron isotope studies of magnetite produced by magnetotactic bacteria. Science 285, 1892–1896 (1999). · DOI
  15. Frankel, R. B., Blakemore, R. & Wolfe, R. S. Magnetite in freshwater magnetotactic bacteria. Science 203, 1355–1356 (1979). · DOI
  16. Frankel, R. B., Papaefthymiou, G. C., Blakemore, R. P. & O’Brien, W. D. Fe3O4 precipitation in magnetotactic bacteria. Biochim. Biophys. Acta. 763, 147–159 (1983). · DOI
  17. Faivre, D., Böttger, L. H., Matzanke, B. F. & Schüler, 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, 8495–8499 (2007). · DOI
  18. Staniland, S., Ward, B., Harrianson, A., Van der Laan, G. & Telling, N. Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism. Proc. Natl. Acad. Sci. USA 104, 19524–19528 (2007). · DOI
  19. Baumgartner, J. et al. Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates. Proc. Natl. Acad. Sci. USA 110, 14883–14888 (2013). · DOI
  20. Dunin-Borkowski, R. E. et al. Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282, 1868–1870 (1998). · DOI
  21. Lins, U., Mc Cartney, M. C., Farina, M., Frankel, R. B. & Buseck, P. R. Habits of magnetosome crystals in coccoid magnetotactic bacteria. Appl. Environ. Microbiol. 71, 4902–4905 (2005). · DOI
  22. Peyre, H., Duval, P. & Henry, L. Diffraction de Fresnel des électrons diffusés élastiquement et inélastiquement par des écrans semi-transparents. J. Phys. 41, 1353–1360 (1980). · DOI
  23. Pennycook, S. J. Z-Contrast STEM for materials science. Ultramicroscopy 30, 58–69 (1989). · DOI
  24. Nudelman, H. & Zarivach, R. Structure prediction of magnetosome-associated proteins. Front. Microbiol. 5, 9, doi:10.3389/fmicb.2014.00009 (2014). · DOI
  25. Balkwill, D. L., Maratea, D. & Blakemore, R. P. Ultrastructure of a magnetotactic spirillum. J. Bacteriol. 141, 1399–1408 (1980). · DOI
  26. Komeili, A., Li, Z., Newman, D. K. & Jensen, G. J. Magnetosomes are cell membrane invaginations organized by the actin-like protein mamk. Science 311, 242–245 (2006). · DOI
  27. Gorby, Y. A., Beveridge, T. J. & Blakemore, R. P. Characterization of the bacterial magnetosome membrane. J. Bacteriol. 170, 834–841 (1988). · DOI
  28. Andersen, O. S. & Koeppe, R. E. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36, 107–130 (2007). · DOI
  29. Taoka, A. et al. Spatial localizations of Mam22 and Mam12 in the magnetosomes of Magnetospirillum magnetotacticum. J. Bacteriol. 188, 3805–3812 (2006). · DOI
  30. Yamamoto, D. et al. Visualization and structural analysis of the bacterial magnetic organelle magnetosome using atomic force microscopy. Proc. Natl. Acad. Sci. USA 107, 9382–9387 (2010). · DOI
  31. Taylor, A. P. & Barry, J. C. Magnetosomal matrix: ultrafine structure may template biomineralization of magnetosomes. J. Microsc. 213, 180–197 (2004). · DOI
  32. Schüler, D. & Baeuerlein, E. Dynamics of iron uptake and Fe3O4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J. Bacteriol. 180, 159–162 (1998). · DOI
  33. Meghan, E. B. et al. Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bulletshaped magnetosomes. Proc. Natl. Acad. Sci. USA 107, 12263–12268 (2010). · DOI
  34. Lefèvre, C. T. et al. Morphological features of elongated-anisotropic magnetosome crystals in magnetotactic bacteria of the Nitrospirae phylum and the Deltaproteobacteria class. Earth Planet. Sci. Lett. 312, 194–200 (2011). · DOI
  35. Frankel, R. B. & Papaefthymiou, G. C. Biomineralization of Fe3O4 in bacteria. Chemical mossbauer spectroscopy (ed. Herber, R. H.) 113–132 (Plenum Press, New York, 1984). · DOI
  36. Abreu, F. et al. Cryo-electron tomography of the magnetotactic vibrio Magnetovibrio blakemorei: Insights into the biomineralization of prismatic magnetosomes. J. Struct. Biol. 181, 162–168 (2013). · DOI
  37. Lins, U. et al. Simple homemade apparatus for harvesting uncultured magnetotactic microorganisms. Braz. J. Microbiol. 34, 111–116 (2003). · DOI
  38. Morillo, V. et al. Isolation, cultivation and genomic analysis of magnetosome biomineralization genes of a new genus of South-seeking magnetotactic cocci within the Alphaproteobacteria. Front. Microbiol. 5, 72, doi:10.3389/fmicb.2014.00072 (2014). · DOI
  39. Silva, K. T. et al. Optimization of magnetosome production and growth by the magnetotactic vibrio Magnetovibrio blakemorei strain MV-1 through a statistics-based experimental design. Appl. Environ. Microbiol. 79, 2823–2827 (2013). · DOI
  40. Fdez-Gubieda, M. et al. Magnetite Biomineralization in Magnetospirillum gryphiswaldense: Time-Resolved Magnetic and Structural Studies. ACS Nano. 7, 3297–3305 (2013). · DOI

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    “This biomineralization also occurs within intracellular membranous vesicles that originate from invaginations of the cytoplasmic membrane [139].”
    Background

See all 20

Metadata

Authors
Werckmann, J., Cypriano, J., Lefèvre, C. T., Dembelé, K., Ersen, O., Bazylinski, D. A., Lins, U., & Farina, M.
Affiliations
  • Universidade Federal do Rio de Janeiro (BR)
  • Centre National de la Recherche Scientifique (FR)
  • University of Nevada, Las Vegas (US)
Corresponding author
Werckmann, Jacques
Venue
Scientific Reports
Published
2017-08-15
Volume
7
Issue
1
Pages
8291-8291
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2744758543
Cited by
20
References
1
Citations by year
2025: 2 · 2024: 5 · 2023: 2 · 2022: 3 · 2021: 2 · 2020: 3 · 2019: 3
FWCI
0.67
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • Digital Scholarship - UNLV (University of Nevada Reno) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (1423939)
  • Agence Nationale de la Recherche (ANR-16-TERC-0025)
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico
  • Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
  • Centre National de la Recherche Scientifique
  • Universidade Federal do Rio de Janeiro
Topics
  • Physical Sciences › Earth and Planetary Sciences › Geophysics › Geomagnetism and Paleomagnetism Studies
  • Physical Sciences › Materials Science › Materials Chemistry › Magnetic Properties and Synthesis of Ferrites
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
Keywords
magnetotactic bacteria, magnetite biomineralization, magnetosomes, iron accumulation, crystal nucleation and growth, iron transport, electron energy loss spectroscopy, energy-dispersive X-ray mapping
MeSH terms
Crystallization, Iron, Rhodospirillaceae, Liquid Crystals, Ferrosoferric Oxide, Magnetosomes

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