Visualizing the dynamic polymerization of the bacterial actin-like cytoskeleton for magnetic organelle positioning

MamK, an actin-like protein conserved in magnetotactic bacteria, functions as a cytoskeletal element that positions the magnetosome, a bacterial geomagnetic sensor organelle. Specifically, MamK polymerizes into filaments associated with the magnetosome chain within each cell. The dynamics of these filaments are fundamental to magnetosome organelle positioning. However, the dynamic nature of the polymerized MamK filaments has not been characterized at the molecular level under physiological conditions. In this study, we used high-speed atomic force microscopy (AFM) to characterize the dynamic MamK polymerization process. MamK polymerized as double-helical filaments with a half-helical pitch distance of 41.3 ± 5.1 nm and a filament diameter of 6.3 ± 0.5 nm. The polymerizing MamK filaments elongated at average speeds of 12.4 ± 4.2 nm/min at the fast-growth ends (plus ends) and from - 4.4 to 8.0 nm/min at the slow-growth ends (minus ends) on the mica substrate in the solution containing 3 µM monomeric MamK. High-speed AFM demonstrated that MamK polymerized into dynamic double-helical filaments with polarity similar to that of eukaryotic actin filaments. Understanding the intrinsic dynamics of MamK, a well-conserved actin-like protein in magnetotactic bacteria, is key to elucidating the mechanism of magnetosome positioning in a bacterial cell.