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Magnetic-field induced rotation of magnetosome chains in silicified magnetotactic bacteria

Abstract : Understanding the biological processes enabling magnetotactic bacteria to maintain oriented chains of magnetic iron-bearing nanoparticles called magnetosomes is a major challenge. The study aimed to constrain the role of an external applied magnetic field on the alignment of magnetosome chains in Magnetospirillum magneticum AMB-1 magnetotactic bacteria immobilized within a hydrated silica matrix. A deviation of the chain orientation was evidenced, without significant impact on cell viability, which was preserved after the field was turned-off. Transmission electron microscopy showed that the crystallographic orientation of the nanoparticles within the chains were preserved. Off-axis electron holography evidenced that the change in magnetosome orientation was accompanied by a shift from parallel to anti-parallel interactions between individual nanocrystals. The field-induced destructuration of the chain occurs according to two possible mechanisms: (i) each magnetosome responds individually and reorients in the magnetic field direction and/or (ii) short magnetosome chains deviate in the magnetic field direction. This work enlightens the strong dynamic character of the magnetosome assembly and widens the potentialities of magnetotactic bacteria in bionanotechnology. Since their discovery more than 30 years ago, magnetotactic bacteria have received much attention in the fields of geological, chemical, physical and biological sciences 1-5. However, the processes by which they synthesize iron oxide (or sulphide) magnetic nanoparticles and organize them into chains allowing the cell to orient itself along the geomagnetic field are still far from being fully understood 6-10. It is well-admitted that production of the nano-crystals occurs in specialized organelles, called magnetosomes, formed by a membrane invagination at multiple sites in the cell. However, identifying the proteins controlling nucleation, size, shape and arrangement in chains of the nanocrystals, as well as the mechanisms of action of these proteins, remains a challenging task 11-15. Phenotypic divergences between different species were evidenced 16. In some Magnetospirillum sp. strains, the chain is stabilized along the longitudinal axis of the cell by an organic filament, MamK protein, while the connection of magnetosomes to this structure is provided by a protein MamJ 17,18. The deletion of MamK gene in Magnetospirillum gryphiswaldense MSR-1 leads to short chains separated by gaps devoid of magnetosomes, while the deletion of MamJ induces aggregation of magnetosomes within the cell with observable filaments not attached to the biogenic particles 19,20. In Magnetospirillum magneticum AMB-1, additional MamJ-like and MamK-like proteins were identified that are involved in the dynamic of the filament and the magnetosome organization in chain 21-23. The capacity of the magnetosome chain to act as a compass is not only related to the spatial arrangement of nanocrystals, but also to their crystallographic and magnetic alignment. In some magnetotactic bacteria (e.g., Magnetospirillum sp.), the biogenic magnetite nanoparticles have a cubo-octahedral morphology with a magnetic
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Marine Blondeau, Yohan Guyodo, François Guyot, Christophe Gatel, Nicolas Menguy, et al.. Magnetic-field induced rotation of magnetosome chains in silicified magnetotactic bacteria. Scientific Reports, Nature Publishing Group, 2018, 8 (1), ⟨10.1038/s41598-018-25972-x⟩. ⟨hal-02124288⟩

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