Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria

A Corrigendum to this article was published on 11 May 2006

Abstract

Magnetotactic bacteria are widespread aquatic microorganisms that use unique intracellular organelles to navigate along the Earth's magnetic field. These organelles, called magnetosomes, consist of membrane-enclosed magnetite crystals that are thought to help to direct bacterial swimming towards growth-favouring microoxic zones at the bottom of natural waters1. Questions in the study of magnetosome formation include understanding the factors governing the size and redox-controlled synthesis of the nano-sized magnetosomes and their assembly into a regular chain in order to achieve the maximum possible magnetic moment, against the physical tendency of magnetosome agglomeration. A deeper understanding of these mechanisms is expected from studying the genes present in the identified chromosomal ‘magnetosome island’, for which the connection with magnetosome synthesis has become evident2. Here we use gene deletion in Magnetospirillum gryphiswaldense to show that magnetosome alignment is coupled to the presence of the mamJ gene product. MamJ is an acidic protein associated with a novel filamentous structure, as revealed by fluorescence microscopy and cryo-electron tomography. We suggest a mechanism in which MamJ interacts with the magnetosome surface as well as with a cytoskeleton-like structure. According to our hypothesis, magnetosome architecture represents one of the highest structural levels achieved in prokaryotic cells.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Δ mamJ mutant phenotype and intracellular localization of MamJ.
Figure 2: Cryo-electron tomography of wild-type and Δ mamJ cells.
Figure 3: Time course of magnetite formation in wild-type and Δ mamJ cells after induction.
Figure 4: Model for magnetosome chain assembly.

References

  1. Bazylinski, D. A. & Frankel, R. B. Magnetosome formation in prokaryotes. Nature Rev. Microbiol. 2, 217–230 (2004)

    CAS  Article  Google Scholar 

  2. Ullrich, S., Kube, M., Schübbe, S., Reinhardt, R. & Schüler, D. A hypervariable 130 kb genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island, which undergoes frequent rearrangements during stationary growth. J. Bacteriol. 187, 7176–7184 (2005)

    CAS  Article  Google Scholar 

  3. Bazylinski, D. Structure and function of the bacterial magnetosome. ASM News 61, 337–343 (1995)

    Google Scholar 

  4. Bazylinski, D. A., Garratt-Reed, A. J. & Frankel, R. B. Electron-microscopic studies of magnetosomes in magnetotactic bacteria. Microsc. Res. Tech. 27, 389–401 (1994)

    CAS  Article  Google Scholar 

  5. Dunin-Borkowski, R. E. et al. Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282, 1868–1870 (1998)

    ADS  CAS  Article  Google Scholar 

  6. Kirschvink, J. L. Paleomagnetic evidence for fossil biogenic magnetite in western Crete. Earth Planet. Sci. Lett. 59, 388–392 (1982)

    ADS  Article  Google Scholar 

  7. Vali, H. & Kirschvink, J. L. in Iron Biominerals (eds Frankel, R. B. & Blakemore, R. P.) 97–116 (Plenum Press, New York and London, 1991)

    Book  Google Scholar 

  8. Grünberg, K. et al. Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70, 1040–1050 (2004)

    Article  Google Scholar 

  9. Evans, J. S. ‘Apples’ and ‘oranges’: comparing the structural aspects of biomineral- and ice-interaction proteins. Curr. Opin. Colloid Interf. Sci. 8, 48–54 (2003)

    CAS  Article  Google Scholar 

  10. Schüler, D., Uhl, R. & Baeuerlein, E. A simple light-scattering method to assay magnetism in Magnetospirillum gryphiswaldense. FEMS Microbiol. Lett. 132, 139–145 (1995)

    Article  Google Scholar 

  11. Philipse, A. P. & Maas, D. Magnetic colloids from magnetotactic bacteria: Chain formation and colloidal stability. Langmuir 18, 9977–9984 (2002)

    CAS  Article  Google Scholar 

  12. Komeili, A., Vali, H., Beveridge, T. J. & Newman, D. K. Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc. Natl Acad. Sci. USA 101, 3839–3844 (2004)

    ADS  CAS  Article  Google Scholar 

  13. Schübbe, S. et al. Characterization of a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J. Bacteriol. 185, 5779–5790 (2003)

    Article  Google Scholar 

  14. Kürner, J., Frangakis, A. S. & Baumeister, W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307, 436–438 (2005)

    ADS  Article  Google Scholar 

  15. Errington, J. Dynamic proteins and a cytoskeleton in bacteria. Nature Cell Biol. 5, 175–178 (2003)

    CAS  Article  Google Scholar 

  16. Schüler, D. Molecular analysis of a subcellular compartment: the magnetosome membrane in Magnetospirillum gryphiswaldense. Arch. Microbiol. 181, 1–7 (2004)

    Article  Google Scholar 

  17. Diebel, C. E., Proksch, R., Green, C. R., Nellson, P. & Walker, M. M. Magnetite defines a vertebrate magnetreceptor. Nature 406, 299–302 (2000)

    ADS  CAS  Article  Google Scholar 

  18. Mora, C. V., Davidson, M., Wild, J. M. & Walker, M. M. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004)

    ADS  CAS  Article  Google Scholar 

  19. Sambrook, J. & Russel, D. W. Molecular Cloning: A Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 2001)

    Google Scholar 

  20. Heyen, U. & Schüler, D. Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl. Microbiol. Biotechnol. 61, 536–544 (2003)

    CAS  Article  Google Scholar 

  21. Schultheiss, D. & Schüler, D. Development of a genetic system for Magnetospirillum gryphiswaldense. Arch. Microbiol. 179, 89–94 (2003)

    CAS  Article  Google Scholar 

  22. Schultheiss, D., Kube, M. & Schüler, D. Inactivation of the flagellin gene flaA in Magnetospirillum gryphiswaldense results in non-magnetotactic mutants lacking flagellar filaments. Appl. Environ. Microbiol. 70, 3624–3631 (2004)

    CAS  Article  Google Scholar 

  23. Grimm, R., Typke, D., Barmann, M. & Baumeister, W. Determination of the inelastic mean free path in ice by examination of tilted vesicles and automated most probable loss imaging. Ultramicroscopy 63, 169–179 (1996)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank P. Graumann for advice on fluorescence microscopy and F. Widdel for helpful comments. This research was supported by the Max Planck Society and the Biofuture program of the Bundesministerium für Bildung und Forschung. Author Contributions A.S. carried out all genetic and growth experiments and performed fluorescence and TEM microscopy. M.G. carried out cryo-electron tomography and analysis of tomograms. D.F. participated in induction experiments. A.L. participated in three-dimensional visualization. J.M.P. directed cryo-electron tomography, EFTEM experiments and data analysis. D.S. coordinated the study and with A.S. finalized the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dirk Schüler.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure Legends

Text to accompany the below Supplementary Figures. (DOC 26 kb)

Supplementary Figure 1

Domain structure of the MamJ protein (PDF 224 kb)

Supplementary Figure 2

Molecular organization of the mamAB cluster in the wild type and δmamJ (PDF 13 kb)

Supplementary Figure 3

Cryo-ET of a wild type cell showing a chain of mature magnetosome crystals located adjacent to the cytoplasmic membrane (PDF 1853 kb)

Supplementary Video 1

Three-dimensional reconstruction of magnetosome organization along a cytoskeleton-like structure in a wild-type M. gryphiswaldense cell obtained by Cryo-ET. (MOV 9703 kb)

Supplementary Video Legend

Text to accompany the above Supplementary Video. (DOC 23 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Scheffel, A., Gruska, M., Faivre, D. et al. An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440, 110–114 (2006). https://doi.org/10.1038/nature04382

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04382

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing