Abstract

Magnetotactic bacteria orient in magnetic fields with the help of their magnetosome chain, a linear structure of membrane enclosed magnetic nanoparticles (magnetosomes) anchored to a cytoskeletal filament. Here, we use simulations to study the assembly and the stability of magnetosome chains. We introduce a computational model describing the attachment of the magnetosomes to the filament and their magnetic interactions. We show that the filamentous backbone is crucial for the robust assembly of the magnetic particles into a linear chain, which in turn is key for the functionality of the chain in cellular orientation and magnetically directed swimming. In addition, we simulate the response to an external magnetic field that is rotated away from the axis of the filament, an experimental method used to probe the mechanical stability of the chain. The competition between alignment along the filament and alignment with the external fields leads to the rupture of a chain if the applied field exceeeds a threshold value. These observations are in agreement with previous experiments at the population level. Beyond that, our simulations provide a detailed picture of chain rupture at the single cell level, which is found to happen through two abrupt events, which both depend on the field strength and orientation. The re-formation of the chain structure after such rupture is found to be strongly sped up in the presence of a magnetic field parallel to the filament, an observation that may also be of interest for the design of self-healing materials. Our simulations underline the dynamic nature of the magnetosome chain. More generally, they show the rich complexity of self-assembly in systems with competing driving forces for alignment.

Highlights

  • The cytoskeleton provides a mechanical scaffold for the cell and it is a key player in organising the cellular components [1], While originally considered to be unique to eukaryotes, the important roles of the cytoskeleton are recognized for bacteria [2,3,4,5]

  • Broken magnetosome chains have been observed after the application of a sufficiently strong magnetic field that was rotated with respect to the chain axis, such that the interaction of the magnetic moments of the individual magnetosomes with the external field competes with their interaction with each other [10]

  • Our model describes the magnetostatic interactions between magnetosome particles and between magnetosome particles and an external magnetic field and the binding of the magnetosome particles to the cytoskeletal filament via elastic linkers

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Summary

Introduction

The cytoskeleton provides a mechanical scaffold for the cell and it is a key player in organising the cellular components [1], While originally considered to be unique to eukaryotes, the important roles of the cytoskeleton are recognized for bacteria [2,3,4,5]. Stability of magnetosome chains—A simulation study example is the magnetosome filament in magnetotactic bacteria, which scaffolds the magnetosome chain that provides these cells with a magnetic moment. The magnetosomes are attached to a cytoskeletal filament based on the actin-related protein MamK to form a chain-like assembly that provides the cell with the maximal magnetic moment [7]. In addition to providing a scaffold for the assembly of the magnetosomes, the MamK filament is involved in the reorganization of the magnetosome chain during cell division [8]. The filament stabilizes the magnetosome chain against ring closure, which is favored by the magnetic interactions of the magnetosomes, but would be detrimental for the function of the chain [9]. The organization and the mechanical stability of the magnetosome assembly are directly linked to its function as a cellular navigation device. Broken magnetosome chains have been observed after the application of a sufficiently strong magnetic field that was rotated with respect to the chain axis, such that the interaction of the magnetic moments of the individual magnetosomes with the external field competes with their interaction with each other [10]

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