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  A bacterial cytolinker couples positioning of magnetic organelles to cell shape control

Pfeiffer, D., Toro-Nahuelpan, M., Awal, R. P., Mueller, F.-D., Bramkamp, M., Plitzko, J. M., et al. (2020). A bacterial cytolinker couples positioning of magnetic organelles to cell shape control. Proceedings of the National Academy of Sciences of the United States of America, 117(50), 32086-32097. doi:10.1073/pnas.2014659117.

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 Creators:
Pfeiffer, Daniel1, Author
Toro-Nahuelpan, Mauricio2, Author              
Awal, Ram Prasad1, Author
Mueller, Frank-Dietrich1, Author
Bramkamp, Marc1, Author
Plitzko, Jürgen M.2, Author              
Schueler, Dirk1, Author
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1external, ou_persistent22              
2Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society, ou_1565142              

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Free keywords: FILAMENTS IN-VIVO; MEMBRANE CURVATURE; CYTOSKELETAL PROTEINS; MAGNETOSOME FORMATION; ESCHERICHIA-COLI; ACTIN; MREB; MAMK; APOLIPOPROTEIN; LOCALIZATIONScience & Technology - Other Topics; magnetotaxis; magnetosome; cytoskeleton; MamK; MreB;
 Abstract: Magnetotactic bacteria maneuver within the geomagnetic field by means of intracellular magnetic organelles, magnetosomes, which are aligned into a chain and positioned at midcell by a dedicated magnetosome-specific cytoskeleton, the "magnetoskeleton." However, how magnetosome chain organization and resulting magnetotaxis is linked to cell shape has remained elusive. Here, we describe the cytoskeletal determinant CcfM (curvature-inducing coiled-coil filament interacting with the magnetoskeleton), which links the magneto-skeleton to cell morphology regulation in Magnetospirillum gryphiswaldense. Membrane-anchored CcfM localizes in a filamentous pattern along regions of inner positive-cell curvature by its coiled-coil motifs, and independent of the magnetoskeleton. CcfM overexpression causes additional circumferential localization patterns, associated with a dramatic increase in cell curvature, and magnetosome chain mislocalization or complete chain disruption. In contrast, deletion of ccfM results in decreased cell curvature, impaired cell division, and predominant formation of shorter, doubled chains of magnetosomes. Pleiotropic effects of CcfM on magnetosome chain organization and cell morphology are supported by the finding that CcfM interacts with the magnetoskeleton-related MamY and the actin-like MamK via distinct motifs, and with the cell shape-related cytoskeleton via MreB. We further demonstrate that CcfM promotes motility and magnetic alignment in structured environments, and thus likely confers a selective advantage in natural habitats of magnetotactic bacteria, such as aquatic sediments. Overall, we unravel the function of a prokaryotic cytoskeletal constituent that is widespread in magnetic and nonmagnetic spirilla-shaped Alphaproteobacteria.

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Language(s): eng - English
 Dates: 2020
 Publication Status: Published in print
 Pages: 12
 Publishing info: -
 Table of Contents: -
 Rev. Type: -
 Identifiers: ISI: 000600608300067
DOI: 10.1073/pnas.2014659117
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Title: Proceedings of the National Academy of Sciences of the United States of America
  Other : PNAS
  Other : Proceedings of the National Academy of Sciences of the USA
  Abbreviation : Proc. Natl. Acad. Sci. U. S. A.
Source Genre: Journal
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Publ. Info: Washington, D.C. : National Academy of Sciences
Pages: - Volume / Issue: 117 (50) Sequence Number: - Start / End Page: 32086 - 32097 Identifier: ISSN: 0027-8424
CoNE: https://pure.mpg.de/cone/journals/resource/954925427230