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

Naturevolume 440, pages110–114 (2006)Cite this article

ACorrigendum 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 inMagnetospirillum gryphiswaldense to show that magnetosome alignment is coupled to the presence of themamJ 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.

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

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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

  1. Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359, Bremen, Germany

    André Scheffel, Damien Faivre & Dirk Schüler

  2. Department of Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, D-82152, Martinsried, Germany

    Manuela Gruska, Alexandros Linaroudis & Jürgen M. Plitzko

Authors
  1. André Scheffel
  2. Manuela Gruska
  3. Damien Faivre
  4. Alexandros Linaroudis
  5. Jürgen M. Plitzko
  6. Dirk Schüler

Corresponding author

Correspondence toDirk Schüler.

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Reprints and permissions information is available atnpg.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 themamAB cluster in the wild type andδmamJ (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-typeM. gryphiswaldense cell obtained by Cryo-ET. (MOV 9703 kb)

Supplementary Video Legend

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

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Scheffel, A., Gruska, M., Faivre, D.et al. An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria.Nature440, 110–114 (2006). https://doi.org/10.1038/nature04382

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Editorial Summary

To the ends of the Earth

Aquatic magnetobacteria are able to navigate along Earth's magnetic field thanks to organelles called magnetosomes. In these, magnetite crystals are enclosed in a membrane and arranged in chains so as to act rather like compass needles. A gene cluster in the magnetobacteriumMagnetospirillum gryphiswaldense was recently implicated in magnetosome formation. Now one of its genes,mamJ, is shown to code for a protein similar in structure to those controlling biomineralization in bones. In the absence of this protein, the magnetosomes collapse. MamJ protein seems to act by connecting empty vesicles to the filamentous structure, so that magnetite crystals then grow within the vesicles.

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