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Spatial localization of Mms6 during biomineralization of Fe3O4 nanocrystals in Magnetospirillum magneticum AMB-1

Journal of Materials Research volume 31, pages 527–535 (2016)Cite this article

Abstract

Magnetotactic bacteria mineralize nanometer-size crystals of magnetite (Fe3O4) through a series of protein-mediated reactions that occur inside of organelles called magnetosomes. Mms6 is a transmembrane protein thought to play a key role in magnetite mineralization. We used both electron and fluorescent microscopy to examine the subcellular location of Mms6 protein within single cells of Magnetospirillum magneticum AMB-1 using Mms6-specific antibodies. We also purified magnetosomes from M. magneticum to determine if Mms6 was physically attached to magnetite crystals. Our results show that Mms6 proteins are present during crystal growth, and Mms6 is found in direct contact with the magnetite crystals or within the lipid/protein membrane surrounding the magnetite crystals. Mms6 was not detected at other subcellular locations within the bacteria or isolated fractions. Because Mms6 was found to completely surround the magnetosomes rather than being localized to one specific area of the magnetosome, it appears that this protein could act on the entire magnetite crystal during the biomineralization process. This supports a model in which Mms6 functions to regulate Fe3O4 crystal morphology. This knowledge is important for future in vitro experiments utilizing Mms6 to synthesize tailored nanomagnets with specific physical or magnetic properties.

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References

  1. P. Tartaj, M.P. Morales, T. Gonzalez-Carreno, S. Veintemillas-Verdaguer, and C.J. Serna: Advances in magnetic nanoparticles for biotechnology applications. J. Magn. Magn. Mater. 290, 28 (2005).

    Article  Google Scholar 

  2. T. Matsunaga and A. Arakaki: Molecular bioengineering of bacterial magnetic particles for biotechnological applications. In Magnetoreception and Magnetosomes in Bacteria, D. Schuler ed.; Springer: New York, 2007; p. 227–254.

    Chapter  Google Scholar 

  3. T. Prozorov, P. Palo, L. Wang, M. Nilsen-Hamilton, D. Jones, D. Orr, S.K. Mallapragada, B. Narasimhan, P.C. Canfield, and R. Prozorov: Cobalt ferrite nanocrystals: Out-performing magnetotactic bacteria. ACS Nano 1, 228 (2007).

    Article  CAS  Google Scholar 

  4. Y. Deng, D. Qi, C. Deng, X. Zhang, and D. Zhao: Superparamagnetic high-magnetization microspheres with an Fe3O4-SiO2 core and perpendicularly aligned mesoporous SiO2 shell for removal of microcystins. J. Am. Chem. Soc. 130, 28 (2008).

    Article  CAS  Google Scholar 

  5. J. Lee, Y. Lee, J.K. Youn, H. Bin Na, T. Yu, H. Kim, S. Lee, Y. Koo, J.H. Kwak, H.G. Park, H.N. Chang, M. Hwang, J. Park, J. Kim, and T. Hyeon: Simple synthesis of functionalized superparamagnetic magnetite/silica core/shell nanoparticles and their application as magnetically separable high-performance biocatalysts. Small 4, 143 (2008).

    Article  CAS  Google Scholar 

  6. Y. Wang, Y.W. Ng, Y. Chen, B. Shuter, J. Yi, J. Ding, S. Wang, and S. Feng: Formulation of superparamagnetic iron oxides by nanoparticles of biodegradable polymers for magnetic resonance Imaging. Adv. Funct. Mater. 18, 308 (2008).

    Article  CAS  Google Scholar 

  7. M. Tanaka, A. Arakaki, S.S. Staniland, and T. Matsunaga: Simultaneously discrete biomineralization of magnetite and tellurium nanocrystals in magnetotactic bacteria. Appl. Environ. Microbiol. 76, 5526 (2010).

    Article  CAS  Google Scholar 

  8. Y. Tang, D. Wang, C. Zhou, W. Ma, Y. Zhang, B. Liu, and S. Zhang: Bacterial magnetic particles as a novel and efficient gene vaccine delivery system. Gene Ther. 19, 1187 (2012).

    Article  CAS  Google Scholar 

  9. H.S. Huangand and J.F. Hainfeld: Intravenous magnetic nanoparticle cancer hyperthermia. Int. J. Nanomed. 8, 2521 (2013).

    Google Scholar 

  10. S.C.N. Tangand and I.M.C. Lo: Magnetic nanoparticles: Essential factors for sustainable environmental applications. Water Res. 47, 2613 (2013).

    Article  Google Scholar 

  11. L. Li, J. Ding, and J. Xue: A facile green approach for synthesizing monodisperse magnetite nanoparticles. J. Mater. Res. 25, 810 (2010).

    Article  CAS  Google Scholar 

  12. R.B. Frankel, R.P. Blakemore, and R.S. Wolfe: Magnetite in freshwater magnetotactic bacteria. Science 203, 1355 (1979).

    Article  CAS  Google Scholar 

  13. D.L. Balkwill, D. Maratea, and R.P. Blakemore: Ultrastructure of a magnetotactic spirillum. J. Bacteriol. 141, 1399 (1980).

    Article  CAS  Google Scholar 

  14. B.R. Heywood, D.A. Bazylinski, A. Garrattreed, S. Mann, and R.B. Frankel: Controlled biosynthesis of greigite (Fe3S4) in magnetotactic bacteria. Naturwissenschaften 77, 536 (1990).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. D. Murat, A. Quinlan, H. Vali, and A. Komeili: Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc. Natl. Acad. Sci. U. S. A 107, 5593 (2010).

    Article  CAS  Google Scholar 

  17. M. Naresh, V. Hasija, M. Sharma, and A. Mittal: Synthesis of cellular organelles containing nano-magnets stunts growth of magnetotactic bacteria. J. Nanosci. Nanotechnol. 10, 4135 (2010).

    Article  CAS  Google Scholar 

  18. M. Greenberg, K. Canter, I. Mahler, and A. Tornheim: Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. Biophys. J. 88, 1496 (2005).

    Article  CAS  Google Scholar 

  19. S. Ullrich, M. Kube, S. Schubbe, R. Reinhardt, and D. Schuler: A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J. Bacteriol. 187, 7176 (2005).

    Article  CAS  Google Scholar 

  20. T. Matsunaga, Y. Okamura, Y. Fukuda, A.T. Wahyudi, Y. Murase, and H. Takeyama: Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp strain AMB-1. DNA Res. 12, 157 (2005).

    Article  CAS  Google Scholar 

  21. A. Komeili, H. Vali, T.J. Beveridge, and D.K. Newman: Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc. Natl. Acad. Sci. U. S. A. 101, 3839 (2004).

    Article  CAS  Google Scholar 

  22. C.T. Lefevreand and L. Wu: Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol. 21, 534 (2013).

    Article  Google Scholar 

  23. 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, 8745 (2003).

    Article  CAS  Google Scholar 

  24. T. Prozorov, S.K. Mallapragada, B. Narasimhan, L. Wang, P. Palo, M. Nilsen-Hamilton, T.J. Williams, D.A. Bazylinski, R. Prozorov, and P.C. Canfield: Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv. Funct. Mater. 17, 951 (2007).

    Article  CAS  Google Scholar 

  25. 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. Colloid Interface Sci. 343, 65 (2010).

    Article  CAS  Google Scholar 

  26. J.M. Galloway, A. Arakaki, F. Masuda, T. Tanaka, T. Matsunaga, and S.S. Staniland: Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro. J. Mater. Chem. 21, 15244 (2011).

    Article  CAS  Google Scholar 

  27. M. Tanaka, E. Mazuyama, A. Arakaki, and T. Matsunaga: Mms6 protein regulates crystal morphology during nano-sized magnetite biomineralization in vivo. J. Biol. Chem. 286, 6386 (2011).

    Article  CAS  Google Scholar 

  28. S. Feng, L. Wang, P. Palo, X. Liu, S.K. Mallapragada, and M. Nilsen-Hamilton: Integrated self-assembly of the Mms6 magnetosome protein to form an iron-responsive structure. Int. J. Mol. Sci. 14, 14594 (2013).

    Article  Google Scholar 

  29. A. Taoka, R. Asada, H. Sasaki, K. Anzawa, L-F. Wu, and Y. Fukumori: Spatial localizations of Mam22 and Mam12 in the magnetosomes of Magnetospirillum magnetotacticum. J. Bacteriol. 188, 3805 (2006).

    Article  CAS  Google Scholar 

  30. Y. Amemiya, A. Arakaki, S.S. Staniland, T. Tanaka, and T. Matsunaga: Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6. Biomaterials 28, 5381 (2007).

    Article  CAS  Google Scholar 

  31. A. Arakaki, A. Yamagishi, A. Fukuyo, M. Tanaka, and T. Matsunaga: Co-ordinated functions of Mms proteins define the surface structure of cubo-octahedral magnetite crystals in magnetotactic bacteria. Mol. Microbiol. 93, 554 (2014).

    Article  CAS  Google Scholar 

  32. L. Wang, T. Prozorov, P.E. Palo, X. Liu, D. Vaknin, R. Prozorov, S. Mallapragada, and M. Nilsen-Hamilton: Self-assembly and biphasic iron-binding characteristics of Mms6, a bacterial protein that promotes the formation of superparamagnetic magnetite nanoparticles of uniform size and shape. Biomacromolecules 13, 98 (2012).

    Article  Google Scholar 

  33. W. Wang, W. Bu, L. Wang, P.E. Palo, S. Mallapragada, M. Nilsen-Hamilton, and D. Vaknin: Interfacial properties and iron binding to bacterial proteins that promote the growth of magnetite nanocrystals: X-ray reflectivity and surface spectroscopy studies. Langmuir 28, 4274 (2012).

    Article  CAS  Google Scholar 

  34. C. Valverde-Tercedor, F. Abadía-Molina, M. Martinez-Bueno, E. Pineda-Molina, L. Chen, Z. Oestreicher, B.H. Lower, S.K. Lower, D.A. Bazylinski, and C. Jimenez-Lopez: Subcellular localization of the magnetosome protein MamC in the marine magnetotactic bacterium Magnetococcus marinus strain MC-1 using immunoelectron microscopy. Arch. Microbiol. 196, 481 (2014).

    Article  CAS  Google Scholar 

  35. M. Richter, M. Kube, D.A. Bazylinski, T. Lombardot, F.O. Gloeckner, R. Reinhardt, and D. Schueler: Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J. Bacteriol. 189, 4899 (2007).

    Article  CAS  Google Scholar 

  36. A. Komeili, Z. Li, D.K. Newman, and G.J. Jensen: Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311, 242 (2006).

    Article  CAS  Google Scholar 

  37. A. Lohße, S. Borg, O. Raschdorf, I. Kolinko, É. Tompa, M. Pósfai, D. Faivre, J. Baumgartner, and D. Schüler: Genetic dissection of the mamAB and mms6 operons reveals a gene set essential for magnetosome biogenesis in Magnetospirillum gryphiswaldense. J. Bacteriol. 196, 2658 (2014).

    Article  Google Scholar 

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ACKNOWLEDGMENTS

This research was supported by the U.S. National Science Foundation grants EAR1424138 and EAR1423939. We would like to thank Marit Nilsen-Hamilton and Pierre Palo for providing us with the plasmid used in this study and their assistance with protein purification; Sara Cole and Richard Montione at The Ohio State University Campus Microscopy and Imaging Facility for their assistance with the microscopy; and Todd Matulnik for assisting us with the batch culturing of M. magneticum AMB-1.

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Authors and Affiliations

  1. School of Natural System, College of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192, Japan

    Zachery Oestreicher

  2. School of Environment and Natural Resources, The Ohio State University, Columbus, Ohio, 43210, USA

    Zachery Oestreicher, Steven K. Lower & Brian H. Lower

  3. School of Earth Sciences, The Ohio State University, Columbus, Ohio, 43210, USA

    Eric Mumper & Steven K. Lower

  4. Department of Chemistry, Columbia Basin College, Pasco, Washington, 99301, USA

    Carol Gassman

  5. School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, Nevada, 89154, USA

    Dennis A. Bazylinski

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  1. Zachery Oestreicher
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  2. Eric Mumper
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Correspondence to Brian H. Lower.

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Oestreicher, Z., Mumper, E., Gassman, C. et al. Spatial localization of Mms6 during biomineralization of Fe3O4 nanocrystals in Magnetospirillum magneticum AMB-1. Journal of Materials Research 31, 527–535 (2016). https://doi.org/10.1557/jmr.2016.41

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