Magnetosome chains are recruited to cellular division sites and split by asymmetric septation

Authors

  • Emanuel Katzmann,

    1. Ludwig-Maximilians-Universität München, Department Biology I, Biozentrum, D-82152 Planegg-Martinsried, Germany
    2. Max Planck Institute of Biochemistry, Department of Molecular Structural Biology, D-82152 Planegg-Martinsried, Germany
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  • Frank D. Müller,

    1. Ludwig-Maximilians-Universität München, Department Biology I, Biozentrum, D-82152 Planegg-Martinsried, Germany
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  • Claus Lang,

    1. Ludwig-Maximilians-Universität München, Department Biology I, Biozentrum, D-82152 Planegg-Martinsried, Germany
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    • Present address: Department of Biology, Stanford University, Stanford, CA 94305, USA.

  • Maxim Messerer,

    1. Ludwig-Maximilians-Universität München, Department Biology I, Biozentrum, D-82152 Planegg-Martinsried, Germany
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  • Michael Winklhofer,

    1. Ludwig-Maximilians-Universität München, Department of Earth and Environmental Sciences, D-80333 Munich, Germany
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  • Jürgen M. Plitzko,

    1. Max Planck Institute of Biochemistry, Department of Molecular Structural Biology, D-82152 Planegg-Martinsried, Germany
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  • Dirk Schüler

    Corresponding author
    1. Ludwig-Maximilians-Universität München, Department Biology I, Biozentrum, D-82152 Planegg-Martinsried, Germany
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E-mail dirk.schueler@lrz.uni-muenchen.de; Tel. (+49) 89218074502; Fax (+49) 89218074515.

Summary

Magnetotactic bacteria navigate along magnetic field lines using well-ordered chains of membrane-enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time-lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole-to-midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division-inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin-like cytoskeletal magnetosome filament. Cryo-electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co-ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria.

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