From invagination to navigation: The story of magnetosome-associated proteins in magnetotactic bacteria

Abstract

Magnetotactic bacteria (MTB) are a group of Gram-negative microorganisms that are able to sense and change their orientation in accordance with the geomagnetic field. This unique capability is due to the presence of a special suborganelle called the magnetosome, composed of either a magnetite or gregite crystal surrounded by a lipid membrane. MTB were first detected in 1975 and since then numerous efforts have been made to clarify the special mechanism of magnetosome formation at the molecular level. Magnetosome formation can be divided into several steps, beginning with vesicle invagination from the cell membrane, through protein sorting, followed by the combined steps of iron transportation, biomineralization, and the alignment of magnetosomes into a chain. The magnetosome-chain enables the sensing of the magnetic field, and thus, allows the MTB to navigate. It is known that magnetosome formation is tightly controlled by a distinctive set of magnetosome-associated proteins that are encoded mainly in a genomically conserved region within MTB called the magnetosome island (MAI). Most of these proteins were shown to have an impact on the magnetism of MTB. Here, we describe the process in which the magnetosome is formed with an emphasis on the different proteins that participate in each stage of the magnetosome formation scheme.

Keywords: biomineralization; magnetic nanoparticles; magnetosome; magnetotactic bacteria; protein function.

Figure 1

Magnetotactic bacterium. (A) Transmission electron microscope (TEM) image of Magnetospirillum gryphiswaldense MSR‐1, contributed by Dr. René Uebe and Dr. Dirk Schüler. The black arrow points toward the magnetosome chain. (B) Magnified illustration of the black box in A: magnetosomes are made of magnetic particles surrounded by a lipid membrane—which invaginate from the cell membrane—and organized as a chain on filaments.

Figure 2

Schematic model of magnetosome formation. Proteins (each is presented in a different shape or color) can be roughly divided into different stages of magnetosome formation (TM proteins cross the membrane; proteins’ sizes, shapes, colors and locations are meaningless, unless specified): (A) MamB, I, L, Q, and Y were suggested to take part in magnetosome invagination, and MamA and E in protein sorting. (B) MamK and J participate in magnetosome alignment into chains. (C) MamB, E, H, M, N, O, P, T, X, Z, and FtsZm are involved in processes such as iron transport, nucleation and chemical environment control. (D) MamC, D, G, F, R, S, Mms6 and MmsF all influence the magnetic particle size and morphology. MamC, D, G and Mms6 locations correspond to the presumed locations in the magnetosome.