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Magnetosome formation in prokaryotes

Key Points

  • Magnetotactic bacteria are motile, generally aquatic microorganisms that can move along geomagnetic field lines. This group of fastidious prokaryotes is heterogeneous and all magnetotactic bacteria identified so far are Gram-negative.

  • Magnetotactic bacteria behave essentially like miniature magnetic compass needles and can respond to the Earth's geomagnetic field because they synthesize intracellular structures, known as magnetosomes, which contain magnetic mineral crystals. Iron oxide magnetosomes contain magnetite (Fe3O4) crystals and iron sulphide magnetosomes contain greigite (Fe3S4) crystals.

  • In their aquatic habitats, most magnetotactic bacteria are found at the oxic–anoxic interface. Magnetotaxis is believed to function in conjunction with aerotaxis to guide magnetotactic bacteria to areas of correct oxygen tension. There are two different mechanisms of magneto-aerotaxis: polar magneto-aerotaxis, in which the magnetic field provides an axis and a direction for motility, and axial-magneto-aerotaxis, in which the magnetic field only provides an axis for motility.

  • The formation of magnetosomes — which are surrounded by a lipid bilayer approximately 3–4 nm thick — is a complex process, involving several discrete steps. At present, there is no evidence to indicate that magnetotactic bacteria use unique iron-uptake systems; evidence for the presence of siderophores in some magnetotactic species, including Magnetospirillum magnetotacticum and Magnetospirillum magneticum, indicates that Fe(III) can be taken up as well as Fe(II). As yet it is unclear whether the magnetosome membrane vesicle is produced before the magnetic crystals have been formed, or whether the cytoplasmic membrane invaginates around the developing crystal.

  • For many years, the inability of researchers to manipulate magnetotactic bacteria genetically hindered progress in elucidating the pathways that are involved in magnetosome synthesis. However, genetic systems for some magnetotactic bacteria have now been established. Additionally, genome sequencing of several species of magnetotactic bacteria is underway.

Abstract

Magnetotactic bacteria were discovered almost 30 years ago, and for many years and many different reasons, the number of researchers working in this field was few and progress was slow. Recently, however, thanks to the isolation of new strains and the development of new techniques for manipulating these strains, researchers from several laboratories have made significant progress in elucidating the molecular, biochemical, chemical and genetic bases of magnetosome formation and understanding how these unique intracellular organelles function. We focus here on this progress.

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Figure 1: Transmission electron micrograph of a negatively stained cell of a typical magnetotactic bacterium.
Figure 2: Anisotropic crystal habits of Fe3O4 crystals.
Figure 3: Electron holography of a region of the magnetosome chain in Magnetospirillum magnetotacticum.
Figure 4: Magneto-aerotaxis.
Figure 5: Transmission electron micrograph of a thin section of a magnetosome chain in a cell of the marine spirillum strain MV-4.
Figure 6: Schematic of possible reactions leading to magnetite biomineralization in known, cultured species of magnetotactic bacteria.
Figure 7: The effects of a magnetosome membrane protein, Mms6, on magnetite formation.

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Acknowledgements

We acknowledge our students, postdoctoral researchers and numerous collaborators, and are particularly grateful for the support of the US National Science Foundation and the National Aeronautics and Space Administration. We thank Y. Fukumori for valuable discussions and suggestions; T. Matsunaga and Y. Okamura for the use of Figure 7; and D. Moyles and T. J. Beveridge for superb electron microscopy.

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Correspondence to Dennis A. Bazylinski.

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Supplementary information

Online Movie 1

This sequence shows magnetotactic spirilla displaying axial magnetotaxis, that is, the magnetic field provides an axis for motility and the direction is determined by aerotaxis. In this homogenous medium, the cells are swimming in both directions along the magnetic field. Movie previously published in Spring, S. & Bazylinski, D. A. in The Prokaryotes (eds Dworkin, M. et al.) © Springer (2000). http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?c hapnum=281&initsec=04_02 (MP4 96 kb)

Online Movie 2

This sequence shows magnetotactic cocci displaying polar magnetotaxis, that is, both the axis and direction of motility are determined by the magnetic field. It can be seen that the cells change direction when the magnetic field is reversed. Movie previously published in Spring, S. & Bazylinski, D. A. in The Prokaryotes (eds Dworkin, M. et al.) © Springer (2000). http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=281&initsec=04_02 (MP4 108 kb)

To view this movie you need Quicktime. To download this player for free click here: Download Quicktime player .

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DATABASES

Entrez

MFT1

SwissProt

MagA

MamA

MamB

MamC

MamD

Mam22

Mms5

Mms6

Mms7

Mms13

Mms16

FURTHER INFORMATION

Joint Genome Institute

Magnetococcus MC-1 sequence

Magnetospirillum magnetotacticum sequence

Magnetotactic bacteria

Richard B. Frankel's laboratory

Glossary

FASTIDIOUS PROKARYOTES

Bacteria that are difficult to cultivate owing to unusual or numerous growth requirements.

VIBRIOID

Used to describe a rod-shaped bacterium that is curved.

TACTIC

Displays movement towards (positive taxis) or away (negative taxis) from a stimulus.

OXIC–ANOXIC INTERFACE

The microaerobic boundary between oxygenated and anaerobic water in an aquatic environment that contains a vertical oxygen gradient.

OBLIGATE MICROAEROPHILE

A bacterium that grows aerobically but only at low, less-than-atmospheric concentrations of oxygen.

PROTEOBACTERIA

An assemblage of metabolically diverse Gram-negative prokaryotes in the domain Bacteria that are separated into five subdivisions: α, β, γ, δ and ε.

MAGNETIC REMANENCE

The net magnetic dipole moment of a magnetic structure after the removal of an external magnetic field.

MAGNETIC DIPOLE MOMENT

An elementary magnetic structure, such as a compass magnet, with north and south magnetic poles that experiences a torque in a uniform magnetic field.

ANISOTROPY

Magnetic properties that vary with the direction of an applied magnetic field relative to the crystallographic direction are said to exhibit anisotropy.

ELECTRON HOLOGRAPHY

An electron interference technique in a transmission electron microscope that is sensitive to magnetic fields in the sample. Analysis of the interference pattern allows visualization of the magnetic field lines.

AEROTAXIS

Motility towards or away from different concentrations of oxygen.

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Bazylinski, D., Frankel, R. Magnetosome formation in prokaryotes. Nat Rev Microbiol 2, 217–230 (2004). https://doi.org/10.1038/nrmicro842

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