Abstract
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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0290-1) contains supplementary material, which is available to authorized users.
Highlights
The navigation of magnetotactic bacteria relies on specific intracellular organelles, the magnetosomes, which are membrane-enclosed crystals of magnetite aligned into a linear chain
We found that the magnetosome chain (MC) dynamic pole-to-midcell motion into daughter cells depends directly on the dynamics of MamK filaments, which seem to originate at the cell pole undergoing a treadmilling growth from the pole towards midcell
Magnetosome chains undergo a rapid and dynamic poleto-midcell repositioning which becomes impaired by the MamKD161A amino acid exchange To assess the MC localization through the cell cycle, we performed in vivo time-lapse fluorescence imaging of EGFP tagged to MamC [26] in synchronized cells of Magnetospirillum gryphiswaldense MSR-1 (MSR)
Summary
The navigation of magnetotactic bacteria relies on specific intracellular organelles, the magnetosomes, which are membrane-enclosed crystals of magnetite aligned into a linear chain. MamK filaments were speculated to recruit the magnetosome chain to cellular division sites, ensuring equal organelle inheritance. It only recently became apparent that bacteria possess organelles [5, 6] and homologs of eukaryotic cytoskeletal proteins such as tubulin, intermediate filaments and several actin families [7,8,9]. As in eukaryotes, during cell division, the equipartitioning of plasmids, chromosomes and organelles has to be carefully controlled to ensure viability and fitness of the offspring throughout the entire bacterial life cycle. Only few examples of organelle or protein cluster segregation in bacteria have been studied in some detail. The fundamental mechanisms of bacterial organelle segregation have remained largely unknown
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