Magnetotaxis in Prokaryotes

Abstract

Magnetotaxis refers to the behaviour of some motile, aquatic bacteria that orient and swim along magnetic field lines. These microorganisms, called magnetotactic bacteria (MTB), contain intracellular structures known as magnetosomes, which are nano‐sized, magnetic, iron‐mineral crystals, each enveloped by a biological (phospholipid bilayer) membrane. Magnetosomes are usually arranged in chains within the cell, providing it with a permanent magnetic dipole moment that facilitates these bacteria in locating and maintaining an optimal, preferred position in chemically stratified aquatic habitats having vertical chemical (e.g. O2) gradients. For many MTB, this is at or below the oxic–anoxic interface in the water column or sediment. Although all MTB are motile by means of flagella and have a cell wall structure characteristic of Gram‐negative bacteria, their diversity is reflected in them possessing a large number of different morphotypes and phylotypes in diverse aquatic environments. Recently, magnetotaxis has been described in microorganisms (protozoa) belonging to the Domain Eukarya, revealing a complex scenario regarding the evolution of magnetic field orientation, in which symbioses between magnetosome‐producing bacteria and cells without magnetosomes should be considered.

Key Concepts

  • Some prokaryotes (bacteria), like eukaryotes, internally compartmentalise and contain organelles.
  • The prokaryotic flagellum in magnetotactic bacteria rotates clockwise and counter‐clockwise thereby propelling the cell forwards and backwards during swimming.
  • Magnetotaxis appears to be a mechanism to make bacterial chemotaxis more effective using the Earth's geomagnetic field. This behaviour can be observed under the microscope by controlling bacterial motility through an artificial magnetic field (magnet).
  • Magnetotactic bacteria contain intracellular, nano‐scale, membrane‐enveloped, magnetic iron‐mineral crystals called magnetosomes.
  • Magnetosomes impart a permanent magnetic dipole moment to cells of magnetotactic bacteria causing them to behave as miniature, motile, compass needles.
  • Magnetotaxis works in conjunction with aerotaxis, and possibly other forms of chemotaxis, to increase energy transduction in magnetotactic bacteria.
  • Genes for magnetosome formation are generally clustered in the genomes of magnetotactic bacteria.
  • Magnetotactic bacteria are important in the cycling of a number of important elements including carbon, iron, nitrogen and sulfur.

Keywords: aerotaxis; biomineralisation; chemically stratified environments; flagellar motion; greigite; magnetite; magnetosome; magnetotactic bacteria; magnetotaxis

Figure 1. Schematic representation of MTB distribution in the Domain Bacteria based on 16S ribosomal ribonucleic acid (rRNA) gene sequences, showing the type of magnetosome biomineralised by members of each taxon.
Figure 2. Differential interface contrast (DIC) light microscopy of uncultured magnetotactic multicellular prokaryotes (MMP).
Figure 3. (a) Differential interface contrast (DIC) light micrograph of North‐seeking (NS) MTB, with polar magnetotaxis, aggregated at the edge of the drop of a ‘hanging drop’. (b) Magnetic enrichment of MTB from an environmental sample by applying the south pole of a magnet (M) several centimetres above the water‐sediment interface for 30 minutes. MTB that have swum towards and accumulated at the magnet are shown as a dark spot at the arrow.
Figure 4. Transmission electron micrograph (TEM) images of magnetotactic bacteria (MTB) and magnetosomes. (a) TEM of a cell of the genus Magnetospirillum showing the chain of magnetosomes within the cell. The magnetite crystals in the magnetosomes have cuboctahedral morphology. The magnetosome chain is fixed in the cell and the interaction between the magnetic dipole moment associated with the chain and the local magnetic field causes the cell to align along magnetic field lines. Rotation of the bipolar flagella (at arrows) causes the cell to swim along the field lines. (b) High‐magnification TEM image of bullet‐ or tooth‐shaped magnetite crystals with one pointed and one flat end or pointed at both ends; (c) High‐magnification TEM image of cuboctahedral magnetite crystals; (d) High‐magnification TEM image of elongated pseudo‐prismatic magnetite crystals; and (e) High‐magnification TEM image of greigite crystals.
Figure 5. Schematic showing the formation of magneto‐aerotactic bands in flat capillary tubes with just one end open placed in a magnetic field B. (a) Diffusion of air into the open end of the capillary results in a O2 concentration gradient in the tube, with the minimum O2 concentration at closed end of the capillary (c, capillary; m, meniscus). (b) Upon magnetic field inversion, bacteria with the axial magneto‐aerotactic mechanism rotate and the band of cells keeps the same position. (c) Under the same conditions, magnetic field inversion results in rotation of the cells by 180o and the band of cells split into two populations in dipolar magnetotaxis (c); while in unipolar magnetotaxis, cells rotate and the band swims either in the same direction into the anoxic zone or the oxic zone (d).
Figure 6. Schematic showing how polar magneto‐aerotaxis helps cells to maintain position at their preferred O2 concentration in the oxic–anoxic interface (OAI) in chemically stratified water columns and sediments (NH, northern hemisphere; SH, southern hemisphere; Bgeo, geomagnetic field). In both hemispheres, cells at higher than optimal O2 concentrations in the ‘oxidised state’ swim forward by rotating their flagella counterclockwise (ccw), whereas cells at lower than optimal O2 concentration in the ‘reduced state’ rotate their flagella clockwise (cw) and swim backward without turning around. Note that the geomagnetic field selects for cells with polarity such that ccw flagellar rotation causes cells to swim downward along the magnetic field lines in both hemispheres.
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Further Reading

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Abreu, Fernanda, Morillo, Viviana, Trubitsyn, Denis, and Bazylinski, Dennis A(May 2020) Magnetotaxis in Prokaryotes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000397.pub3]