Segregation of prokaryotic magnetosomes organelles is driven by treadmilling of a dynamic actin-like MamK filament

BMC Biology

Research Article

Stefan Klumpp¹  Marc Bramkamp²  Frank D. Müller³  Dirk Schüler³  Mauricio Toro-Nahuelpan⁴  Jürgen M. Plitzko⁵ 

[1]Department Theory and Bio-Systems, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany

[2]Institute for Nonlinear Dynamics, Georg August University Göttingen, Göttingen, Germany

[3]Department of Biology I, Ludwig-Maximilians-University Munich, Planegg-Martinsried, Germany

[4]Department of Microbiology, University of Bayreuth, 95447, Bayreuth, Germany

[5]Department of Microbiology, University of Bayreuth, 95447, Bayreuth, Germany

[6]Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Planegg-Martinsried, Germany

[7]Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Planegg-Martinsried, Germany

关键词: Actin;    Bacterial cytoskeleton;    Magnetosomes;    Magnetotactic bacteria;    MamK;    Organelles;    Partitioning;    Prokaryote;    Segregation;   

DOI  :  10.1186/s12915-016-0290-1

 received in 2016-05-23, accepted in 2016-07-29,  发布年份 2016

来源: Springer

【 摘 要 】

BackgroundThe navigation of magnetotactic bacteria relies on specific intracellular organelles, the magnetosomes, which are membrane-enclosed crystals of magnetite aligned into a linear chain. The magnetosome chain acts as a cellular compass, aligning the cells in the geomagnetic field in order to search for suitable environmental conditions in chemically stratified water columns and sediments. During cytokinesis, magnetosome chains have to be properly positioned, cleaved and separated in order to be evenly passed into daughter cells. In Magnetospirillum gryphiswaldense, the assembly of the magnetosome chain is controlled by the actin-like MamK, which polymerizes into cytoskeletal filaments that are connected to magnetosomes through the acidic MamJ protein. MamK filaments were speculated to recruit the magnetosome chain to cellular division sites, thus ensuring equal organelle inheritance. However, the underlying mechanism of magnetic organelle segregation has remained largely unknown.ResultsHere, we performed in vivo time-lapse fluorescence imaging to directly track the intracellular movement and dynamics of magnetosome chains as well as photokinetic and ultrastructural analyses of the actin-like cytoskeletal MamK filament. We show that magnetosome chains undergo rapid intracellular repositioning from the new poles towards midcell into the newborn daughter cells, and the driving force for magnetosomes movement is likely provided by the pole-to-midcell treadmilling growth of MamK filaments. We further discovered that splitting and equipartitioning of magnetosome chains occurs with unexpectedly high accuracy, which depends directly on the dynamics of MamK filaments.ConclusionWe propose a novel mechanism for prokaryotic organelle segregation that, similar to the type-II bacterial partitioning system of plasmids, relies on the action of cytomotive actin-like filaments together with specific connectors, which transport the magnetosome cargo in a fashion reminiscent of eukaryotic actin-organelle transport and segregation mechanisms.

【 授权许可】

CC BY   
© Toro-Nahuelpan et al. 2016