Magnetosome chains are recruited to cellular division sites and split by asymmetric septation

Abstract

SummaryMagnetotactic bacteria navigate along magnetic field lines using well-ordered chains of membraneenclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time-lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole-to-midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division-inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin-like cytoskeletal magnetosome filament. Cryo-electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co-ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria.

Magnetotactic bacteria

“…Importantly, the physical forces can provide new functions, but, at same time, they come with their intrinsic constraints that other cellular processes may have to deal with. Here, a good example is cell division, where attractive magnetic forces must be overcome [19] and the magnetic organization must be preserved in both daughter cells [65]. Swimming of these bacteria is subject to magnetic orientation, which allows to steer them to their preferred habitat, the oxic-anoxic transition zone, as (on the Northern hemisphere) the oxygen gradient in aquatic environments and the magnetic field are antiparallel.…”

“…Thus magnetic forces can be expected to affect intracellular processes, for example during cell division [18,19]. However, the interaction energies and forces are quite sensitive to the distance between the particles and the force decreases quickly if that distance is increased.…”

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

“…The small, hydrophobic proteins MamG, MamF, MamD, and MamC control in a cumulative manner the growth of magnetite crystals (21). Magnetosomes were assembled into chains by the interaction of MamJ with the actin-like MamK filament that is also involved in chain positioning (6,9,58). OM, outer membrane; IM, inner membrane; MP, magnetosome protein.…”

The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

“…This suggests that Magnetospirillum species typically may contain two functional ftsZ genes, one of which encodes a full-length protein while the other always encodes a C-terminally truncated protein. Interestingly, in all magnetospirilla, the truncated genes are part of the conserved mamXY operon within the magnetosome island (MAI) located next to genes exclusively involved in magnetosome formation (17,18), which led to speculation that the truncated ftsZ genes may function in magnetosome synthesis and chain assembly or may be involved in the apparently unusual mechanism of asymmetric cell division and cell bending during cytokinesis in Magnetospirillum species (19,20).…”