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.

The cation diffusion facilitator protein MamM’s cytoplasmic domain exhibits metal-type dependent binding modes and discriminates against Mn2+

“…Magnetotactic bacteria (MTB) are a group of Gram-negative bacteria that align with and move along magnetic fields. The bacterium contains subcellular organelles named magnetosomes, each of which is composed of ~30-120 nm iron-based magnetic particle (magnetite or gregite) enclosed in a protein-rich lipid membrane (Barber-Zucker et al, 2016a;Komeili, 2012;Uebe and Schüler, 2016). The magnetosomes are arranged on an actin-like polymer in a chain arrangement, creating a magnetic dipole moment which allows these bacteria to use external magnetic fields.…”

Structure of the magnetosome‐associated actin‐like MamK filament at subnanometer resolution

“…Magnetotactic bacteria such as Magnetospirillum magneticum AMB‐1 are capable of aligning in the earth's magnetic field, which allows them to swim towards sources of oxygen . This is achieved through the formation of magnetosomes, ∼50 nm membrane‐bound cellular compartments in which single magnetite or greigite crystals are biomineralized . Efficient orientation in magnetic fields arises from alignment of multiple magnetosomes, which are positioned in a linear array that acts much like a compass needle.…”

“…11 This is achieved through the formation of magnetosomes, 50 nm membrane-bound cellular compartments in which single magnetite or greigite crystals are biomineralized. 12,13 Efficient orientation in magnetic fields arises from alignment of multiple magnetosomes, which are positioned in a linear array that acts much like a compass needle. Alignment of magnetosomes is achieved by apparent binding to a cytoplasmic filament consisting of the magnetosome-specific actin homolog MamK.…”

Morphological and cellular diversity of magnetotactic bacteria: A review

“…The main steps in the process of MS formation are membrane invagination, protein sorting, MS alignment into chains, iron transport, redox control, nucleation, magnetic crystal size, and shape control and chain formation as shown in Fig. . Invagination of the CM is the first step during MS formation.…”

“…Faivre et al [75] reported that iron, temperature, and pH have significant impact on physiology of bacterial cell, also on microstructural and physical characteristics of magnetite crystals formed by FIGURE 2 Different steps during magnetosomes (MS) chain formation; reproduced with permission from Ref. [66] MTB. However, studies on environmental conditions of MS synthesis by MTB are limited [75].…”