Unravelling the cytoskeletal network that governs mobility and positioning of magnetic organelles in bacteria: novel players and functions.
Final Report Abstract
Magnetospirillum gryphiswaldense cells, like other magnetotactic bacteria, synthesize membrane enveloped ferromagnetic crystals, so-called magnetosomes. These magnetic organelles are strung to linear chains by interaction with filaments of the actin-like MamK protein through the adapter protein MamJ. Arranging the nanomagnets in this way sums up their single magnetic moment vectors and builds an instrument akin to an intracellular compass-needle which is used by the bacterial cells for efficient navigation in the geomagnetic field. It has been shown that the dynamic MamK filament system plays a key role in segregation of magnetosomes and re-positioning of the split half-chains to midcell upon cell division. However, for quite some time it was not understood how positioning of the magnetosome chain precisely along the motility axis is accomplished within the spiral-shaped cells of M. gryphiswaldense, a prerequisite for optimal performance of the magnetoreception instrument. In the present work, we were able to answer this question. We identified and functionally characterized novel cell topological landmarks, the structural proteins MamY (Nature background) and CcfM (UBT press release), which are part of the intricate cytoskeletal network governing mobility and positioning of magnetosomes. MamY forms a rigid mechanical scaffold that linearly spans the cell along the inner positive membrane curvature (geodetic axis). We demonstrate that interaction of MamY with MamK/J secures the magnetosome chain in perfect alignment with the motility axis of the cell, and propose MamY, K and J as components of a dedicated magnetoskeleton. CcfM was identified as the first ‘cytolinker’ protein between the components of the magnetoskeleton (MamY, K) and intrinsic cytoskeleton components (MreB). It polymerizes membrane-curvature dependently into a pole-to-pole spanning flexible scaffold and couples the positioning of magnetic organelles to the control of helical cell-shape.
Publications
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2019. A gradient forming MipZ protein mediating the control of cell division in the magnetotactic bacterium Magnetospirillum gryphiswaldense. Mol Microbiol
Toro‐Nahuelpan, Mauricio; Corrales‐Guerrero, Laura; Zwiener, Theresa; Osorio‐Valeriano, Manuel; Müller, Frank‐Dietrich; Plitzko, Jürgen M.; Bramkamp, Marc; Thanbichler, Martin & Schüler, Dirk
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2019. MamY is a membrane-bound protein that aligns magnetosomes and the motility axis of helical magnetotactic bacteria. Nature Microbiol 4(11)
Toro-Nahuelpan, Mauricio; Giacomelli, Giacomo; Raschdorf, Oliver; Borg, Sarah; Plitzko, Jürgen M.; Bramkamp, Marc; Schüler, Dirk & Müller, Frank-Dietrich
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2020. A bacterial cytolinker couples positioning of magnetic organelles to cell shape control. Proc. Natl. Acad. Sci. USA
Pfeiffer, Daniel; Toro-Nahuelpan, Mauricio; Awal, Ram Prasad; Müller, Frank-Dietrich; Bramkamp, Marc; Plitzko, Jürgen M. & Schüler, Dirk
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2020. A compass to boost navigation - cell biology of bacterial magnetotaxis. J Bacteriol
Müller, Frank D.; Schüler, Dirk & Pfeiffer, Daniel
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2020. Biosynthesis and intracellular organization of magnetosomes in magnetotactic bacteria. In: D. Jendrossek (ed.) Microbiology monographs, vol. 34: Bacterial organelles and organelle-like inclusions. Springer, Heidelberg, p. 53-70
Schüler, Dirk & Müller, Frank D.
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2020. Genome-wide identification of essential and auxiliary gene sets for magnetosome biosynthesis in Magnetospirillum gryphiswaldense. mSystems
Silva, Karen T.; Schüler, Margarete; Mickoleit, Frank; Zwiener, Theresa; Müller, Frank D.; Awal, Ram Prasad; Weig, Alfons; Brachmann, Andreas; Uebe, René & Schüler, Dirk
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2020. Quantifying the benefit of a dedicated “magnetoskeleton” in bacterial magnetotaxis by live-cell motility tracking and soft agar swimming assay. Appl Environ Microbiol 86:e01976-19
Pfeiffer, Daniel & Schüler, Dirk
