Magnetotaxis in Bacteria

Richard B. Frankel, Department of Physics, Cal Poly State University, San Luis Obispo, CA 93407
Dennis A. Bazylinski, Department of Microbiology, Iowa State University, Ames, IA 50011

1. Magnetotaxis
Magnetotaxis refers to the behavior of some motile, aquatic, bacteria in which they orient and migrate along magnetic field lines (Blakemore, 1982). Magnetotactic bacteria are indigenous in chemically-stratified water columns or sediments where they occur predominantly at the oxic-anoxic transition zone (OATZ) and the anoxic regions of the habitat or both. They represent a diverse group of microorganisms with respect to morphology, physiology and phylogeny (Spring and Bazylinski, 2000). The diversity of magnetotactic bacteria is reflected by the large number of different morphotypes found in environmental samples of water or sediment as well as by the phylogenetic analysis of cultured and uncultured magnetotactic bacteria. Commonly observed morphotypes include coccoid to ovoid cells, rods, vibrios and spirilla of various dimensions. One of the more unique morphotypes is an apparently multicellular bacterium referred to as the many-celled magnetotactic prokaryote (MMP). All magnetotactic bacteria are motile by means of flagella and have a cell wall structure characteristic of Gram-negative bacteria. The arrangement of flagella varies between species/strains and can be either polar, bipolar, or in tufts.

Magnetotactic bacteria
The magnetotactic bacteria are extremely fastidious, difficult to isolate and grow. Thus there are very few axenic cultures of magnetotactic bacteria. Most cultured strains belong to the genus Magnetospirillum. Currently recognized species include M. magnetotacticum strain MS-1, M. gryphiswaldense, and M. magnetotacticum strain AMB-1. Several other freshwater magnetotactic spirilla in pure culture have not yet been completely described (Schüler et al., 1999). Other species of cultured magnetotactic bacteria include a variety of as yet incompletely characterized organisms: the marine vibrios, strains MV-1 and MV-2; a marine coccus, strain MC-1; and a marine spirillum, strain MV-4 (Bazylinski and Frankel, 2000). There is also an anaerobic, sulfate-reducing, rod-shaped bacterium, strain RS-1, that appears to be closely related to the genus Desulfovibrio (Sakaguchi et al., 1993). These cultured organisms, except strain RS-1, are obligate or facultative microaerophiles and all are chemoorganoheterotrophic although the marine strains can also grow chemolithoautotrophically.

A number of uncultured, morphologically conspicuous magnetotactic bacteria have been examined in some detail. A very large, rod-shaped magnetotactic bacterium called Magnetobacterium bavaricum was found to inhabit the OATZ in the sediments of calcareous freshwater lakes in Bavaria. The MMP described above is an aggregation of about 20-30 cells arranged in a roughly spherical manner that moves as an entire unit,.and is phylogenetically associated with the sulfate-reducing bacteria. This organism has been found in marine and brackish aquatic habitats around the world.

Detection of magnetotaxis
An easy assay for magnetotactic bacteria in environmental samples can be made with a standard laboratory microscope with 10x-40x objective. The assay method is to remove a drop of water and sediment from a sample, place it on a microscope slide and place a bar magnet on the microscope stage near the drop so the axis of the magnet is parallel to the plane of the slide and passes through the center of the drop. The magnetic field (B) at the drop should be at least a few gauss and the bar magnet should initially be oriented so that the ësouthí magnetic pole (the pole that attracts the North-indicating end of a magnetic compass needle)* is nearest the drop. Magnetotactic bacteria in the drop can be seen swimming persistently toward or away from the bar magnet and to accumulate along the edge of the drop. If the magnet is now rotated 180°, the bacteria will rotate and swim away from the edge, i.e., they swim in the same direction relative to B. Another 180° rotation of the bar magnet will cause the bacteria to return to the same edge of the drop. Bacteria that swim toward the ësouthí magnetic pole of the bar magnet, i.e., swim parallel to B, are said to have North-seeking (NS) polarity because they would swim northward in the geomagnetic field; bacteria that swim away from the ësouthí magnetic pole (or toward the ënorthí magnetic pole), i.e., swim antiparallel to B, are said to have South-seeking (SS) polarity. Using this assay, it has been found that magnetoactic bacteria from hemisphere habitats are predominantly NS whereas magnetoactic bacteria from Southern hemisphere habitats are predominantly SS.

One modification of the assay is to use a hanging drop on a cover slip placed on a small o-ring on the microscope slide. This eliminates perturbation of the drop by currents in the room and reduces evaporation of the drop. It also allows sediment in the drop to fall to the bottom, leaving the edge of the drop clear to view the bacteria. It is also possible to magnetically enrich for higher numbers of magnetotactic cells by placing the ësouthí pole (in the Northern Hemisphere; the ënorthí pole of the magnet is used in the Southern Hemisphere) of a bar magnet adjacent to the outer surface of the jar containing a sediment and water sample with the axis of the magnet perpendicular to the surface. If magnetotactic bacteria are abundant in the sample they will collect on the inside surface of the jar closest to the bar magnet. They can then be easily removed with a Pasteur pipette and assayed as described above. A more sophisticated setup would utilize either a current carrying coil wound on a soft iron nail or a Helmholtz coil pair with a current reversing switch in place of the bar magnet.

It should be noted that because of diffusion of air into the drop, this assay is carried out under aerobic conditions. It should also be noted that magnetotaxis in this assay involves active swimming by the cells, i.e., the cells are not being pulled or pushed by the magnet. Killed cells in suspension will orient along the magnetic field but will not move along the field. Finally, there are some magnetoactic bacteria, particularly spirilla, that migrate along the magnetic field but swim in either direction with equal probability.

*By definition, a magnetic field points toward the ësouthí magnetic pole of a bar magnet and away from the ënorthí magnetic pole. The geomagnetic pole near the geographic North pole is a ësouthí magnetic pole and the geomagnetic pole near the geographic South is a ënorthí magnetic pole. The geomagnetic field points from the South geomagnetic pole pole towards the North geomagnetic pole. At various times in the distant past the geomagnetic field was reversed and the North and South magnetic poles were ënorthí and ësouthí magnetic poles, respectively.

2. Magnetosomes
All magnetotactic bacteria contain magnetosomes, which are intracellular structures comprising magnetic iron mineral crystals enveloped by a phospholipid membrane Gorby et al., 1988). The magnetosome membrane is presumably a structural entity that anchors the mineral particles at particular locations in the cell, as well as the locus of biological control over the nucleation and growth of the mineral crystal. The magnetosome magnetic mineral phase consists of magnetite, Fe3O4, or greigite, Fe3S4. Each magnetotactic species or strain exclusively produces either magnetite or greigite magnetosomes, except for one marine organism that produces magnetosomes of both kinds. The magnetosome crystals are of order 35 to 120 nm in length, which is within the permanent single-magnetic-domain (SD) size range for both minerals. In the majority of magnetotactic bacteria, the magnetosomes are organized in one or more straight chains of various lengths parallel to the long axis of the cell (Figure 1). Dispersed aggregates or clusters of magnetosomes occur in some magnetotactic bacteria, usually at one side of the cell, which often corresponds to the site of flagellar insertion. The narrow size range and consistent morphologies of the magnetosome crystals in each species or strain are clear indications that the magnetotactic bacteria exert a high degree of control over the processes of magnetosome formation.

Figure 1 Transmission electron micrograph of Magnetospirillum magnetotacticum showing the chain of magnetosomes inside the cell. The magnetite crystals incorporated in the magnetosomes have cuboctaheral morphology and are ca. 42 nm long. 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 be oriented along the magnetic field lines. Rotation of the cellular flagella (not shown) causes the cell to migrate along the field lines. Bar equals 1 micron.

Cellular magnetic dipole
Magnetosomes within the permanent SD size range are uniformly magnetized with the maximum magnetic dipole moment per unit volume. Magnetic crystals larger than SD size are non-uniformly magnetized because of the formation of multiple magnetic domains, domain walls, or vortex configurations; this has the effect of significantly reducing their magnetic dipole moments. On the other hand, very small SD particles are superparamagnetic (SPM). Although SPM particles are still uniformly magnetized, their magnetic dipole moments are not constant because of thermally-induced spontaneous reversals which produce a time-averaged moment of zero. Therefore, magnetotactic bacteria produce the optimum particle size for maximum magnetic dipole moment per magnetosome.

When magnetosomes are arranged in a single chain, as in Magnetospirillum magnetotacticum, magnetostatic interactions between the single-magnetic domain particles cause the particle moments to spontaneously orient parallel to each other along the chain direction (Frankel, 1984). This results in a permanent magnetic dipole for the entire chain of magnetosomes with natural remanent magnetization approaching the saturation magnetization. The permanent magnetic structure of magnetosome chains has been demonstrated by electron holography in the electron microscope, by magnetic force microscopy and by pulsed magnetic field remanence measurements on individual cells.

A chain of ten-twenty 50 nm magnetosomes would be sufficient for orientation of a magnetotactic bacterium along the geomagnetic field at ambient temperature. Since the chain of particles is fixed within the cell, the entire cell is oriented by the torque exerted on the magnetic dipole by the magnetic field. This results in the migration of the cell along the magnetic field as it swims. If the magnetic field is decreased, the time-averaged orientation of the cell along the field is decreased and the migration rate of the cell in the magnetic field direction is decreased, even though the swimming speed of the cell is unchanged.

Magnetite Magnetosomes
High resolution transmission electron microscopy, selected area electron diffraction studies and electron holography have revealed that the magnetite particles within magnetotactic bacteria are of relatively high structural perfection and have been used to determine their idealized morphologies. The morphologies are all derived from combinations of {111}, {110} and {100} forms (a form refers to the equivalent symmetry related lattice planes of the crystal structure) with some distortions. These include cuboctahedral ([100] + [111]), and elongated pseudo-hexahedral or pseudo- octahedral prisms. The cuboctahedral crystal morphology preserves the symmetry of the face-centered cubic spinel structure, i.e., all symmetry related crystal faces develop equally. In the pseudo-hexahedral and pseudo-octahedral prismatic morphologies symmetry related faces develop unequally. This implies anisotropic growth conditions, e.g., a temperature gradient, a chemical concentration gradient, or an anisotropic ion flux.

Greigite Magnetosomes
Virtually all freshwater, magnetotactic bacteria have been found to synthesize magnetite as the mineral phase of their magnetosomes. In contrast, many marine, estuarine, and salt marsh species produce iron sulfide-type magnetosomes consisting primarily of the magnetic iron sulfide, greigite. While none are available in pure culture, recognized greigite-producing magnetotactic bacteria includes the MMP and a variety of relatively large, rod-shaped bacteria. The greigite crystals in their magnetosomes are thought to form from non-magnetic precursors including mackinawite (tetragonal FeS) and possibly a sphalerite-type cubic FeS. Like magnetite crystals in magnetosomes, the morphologies of the greigite crystals also appear to be species and/or strain-specific. There is one reported instance of a marine bacterium that contains magnetite and greigite magnetosomes co-organized within the same magnetosome chain.

3. Function of magnetotaxis
Like most other free-swimming bacteria, magnetotactic bacteria propel themselves through the water by rotating their helical flagella. Because of their magnetosomes, magnetotactic bacteria are passively oriented and actively migrate along the local magnetic field B, which in natural environments is the geomagnetic field. The original model for the function of magnetotaxis was based on the assumption that all magnetotactic bacteria are micro-aerophilic and indigenous in sediments. The geomagnetic field is inclined downward from horizontal in the Northern Hemisphere and upward in the Southern hemisphere, with the inclination magnitude increasing from the equator to the poles. NS Cells which swim northward in the Northern hemisphere and SS cells which swim southward in the Southern hemisphere would migrate downward towards the sediments along the inclined geomagnetic field lines. Thus magnetotaxis helps to guide cells in each hemisphere downward to less oxygenated regions of aquatic habitats. Once cells have reached their preferred microhabitat they would presumably stop swimming and adhere to sediment particles until conditions changed, as for example, when additional oxygen was introduced, or when disturbance of the sediments caused them to be displaced into the water column. This theory is supported by the predominant occurrence of NS magnetotactic bacteria in the Northern hemisphere and SS magnetotactic bacteria in the Southern hemisphere, as determined by the magnetotaxis assay under oxic conditions. Due to the negative and positive sign of the geomagnetic field inclination in the Northern and Southern hemispheres, respectively, magnetotactic bacteria in both hemispheres therefore swim downward toward the sediments under oxic conditions.

The discovery of large populations of magnetotactic bacteria at the OATZ in the water columns of certain chemically stratified aquatic habitats, and the isolation of obligately micro-aerophilic, coccoid magnetotactic bacterial strains, has led to a revised view of magnetotaxis. The original model did not completely explain how bacteria in the anoxic zone of a water column benefit from magnetotaxis, nor did it explain how the magnetotactic cocci form micro-aerophilic bands of cells in semi-solid oxygen gradient medium. When distinct morphotypes of magnetotactic bacteria, isolated and grown in pure culture, were studied in oxygen concentration gradients using thin, flattened capillaries, it became clear that magnetotaxis and aerotaxis work together in these bacteria. The behavior observed in these strains has been referred to as "magneto-aerotaxis", and two different magneto-aerotactic mechanisms, termed polar and axial, are found in different bacterial species (Frankel et al., 1997).

The two mechanisms can be seen in the magnetotaxis assay described in the first section above. The magnetotactic bacteria, principally the magnetotactic cocci (e.g., strain MC-1), that swim persistently in one direction along the magnetic field (NS or SS), are polar magneto-aerotactic. Magnetotactic bacteria, especially the freshwater spirilla (e.g., Magnetospirillum magnetotacticum), that swim in either direction along the magnetic field line with frequent, spontaneous reversals of swimming direction without turning around, and accumulate in approximately equal numbers on both sides of the water drop, are axial magneto-aerotactic. Thus the distinction between NS and SS does not apply to axial magnetotactic-aerotactic bacteria.

The two mechanisms can best be seen in flattened capillary tubes containing suspensions of cells in reduced medium with one or both ends of the capillary tube open in a magnetic field oriented parallel to the capillary. In the situation where one end of the capillary is open and the other sealed, a single, oxygen gradient forms along the tube beginning at the open end of the capillary with the oxygen gradient oriented anti-parallel to the magnetic field. Both cells of Magnetospirillum magnetotacticum and NS cells of strain MC-1 form aerotactic bands below the meniscus at the open end of the capillary, presumably where diffusion of oxygen into the capillary and consumption of oxygen in the band results in a preferred oxygen concentration. Cells can be seen swimming parallel and anti-parallel to the magnetic field through the band in both cases. Reversal of the magnetic field results in 180° rotation of the cells of both type. Whereas the position of the M. magnetotacticum band remains unchanged following the field reversal, the MC-1 band separates into two groups of cells swimming in opposite directions along B, away from the position of the band before the reversal. A second reversal results in the reformation of a single band. In the second situation, where both ends of the capillary tubes are open, diffusion of oxygen into the ends of the tubes creates an oxygen gradient at each end of the tube, oriented in opposite directions relative to B (Figure 2). M. magnetotacticum cells form bands at both ends of the tube, whereas MC-1 cells form an aerotactic band at only one end of the tube, the end for which the direction of increasing oxygen concentration is opposite to B. Thus for polar magnetotactic bacteria the magnetic field provides an axis and direction for motility, whereas for axial magnetotactic bacteria the magnetic field only provides an axis of motility, pointing to the different magneto-aerotactic mechanisms occurring in the two types of bacteria. In both cases, magnetotaxis increases the efficiency of aerotaxis in vertical concentration gradients by reducing a three-dimensional search problem to one dimension.

Figure 2 Schematic showing the formation of magneto-aerotactic bands in flat capillary tubes with both ends open placed in a magnetic field B. (a) Diffusion of air into both ends results in a double oxygen concentration gradient in the tube, with the minimum oxygen concentration at the center (c, capillary; m, meniscus). (b) Bacteria with the axial magneto-aerotactic mechanism form bands at both ends of the tube. (c) Northern hemisphere bacteria with the polar magneto-aerotactic mechanism form a band only at end of the tube for which the B is antiparallel to the oxygen gradient (c). Southern hemisphere bacteria would form a band only at the other end of the tube.

Axial Magneto-aerotaxis mechanism
The aerotactic, axial magnetotactic spirilla appear to locate and remain at a preferred or optimal oxygen concentration, at which the proton motive force generated by the cell is maximal, by means of a temporal sensory mechanism similar to that which occurs in many non-magnetotactic, chemotactic bacteria. Cells sample the oxygen concentration as they swim and compare the present concentration with that in the recent past. The change in oxygen concentration with time is connected to the probability of switching the sense of flagellar rotation (cw or ccw) and hence the direction of migration. Axial magneto-aerotactic cells moving away from the optimal oxygen concentration toward higher or lower oxygen concentration have an increased probability of reversing the sense of flagellar rotation and hence the direction of migration along B which causes them to return to the band. Cells moving toward the optimum oxygen concentration have a decreased probability of reversing the sense of flagellar rotation. At constant oxygen concentration band formation does not occur and the cells revert to an intermediate probability of reversal; this is known as adaptation. In the axial magneto-aerotactic model, the bacteria must be actively motile in order to quickly measure and respond to local concentration gradients. Since the cells use the magnetic field to provide an axis but not a direction of motility, the relative orientation of B and the concentration gradient is unimportant to aerotactic band formation. The combination of a passive alignment along inclined geomagnetic field lines with an active, temporal, aerotactic response provides axial magneto-aerotactic organisms with an efficient mechanism to find the micro-oxic or sub-oxic zone in habitats with vertical, chemical stratification.

Polar Magneto-aerotaxis
The large majority of naturally occurring magnetotactic bacteria display polar magnetotaxis. Although NS cells swim persistently parallel to B under oxic conditions it was demonstrated that under reducing conditions they swim in anti-parallel to B without turning around. This suggests that the sense of flagellar rotation (presumably ccw) is unchanged as long as the cells remain under oxic conditions, and furthermore, that the opposite sense of flagellar rotation (cw) occurs under reducing conditions and likewise remains unchanged as long as the cells remain under reducing conditions. Thus instead of a temporal sensory mechanism, polar magneto-aerotactic cells have a two-state sensory mechanism that determines the sense of flagellar rotation and consequently swimming direction relative to B (Figure 3). Under higher than optimal oxygen tensions, the cell is presumably in an "oxidized state" and cw flagellar rotation causes the cell to migrate persistently parallel to B, i. e., downward in the Northern hemisphere. Under reducing conditions, or sub-optimal oxygen concentrations, the cell switches to a "reduced state", in which cw flagellar rotation causes the cell to migrate anti-parallel to B (upward in the Northern Hemisphere). The two-state sensing mechanism results in an efficient aerotactic response, provided that the oxygen-gradient is oriented vertically so that it is more or less anti-parallel to B, guiding the cell back toward the optimal oxygen concentration from either reducing or oxidizing conditions. This is especially important because adaptation, which would lead to spontaneous reversals of the swimming direction, is never observed in controlled experiments with the cocci. This model accounts for the fact that cells swim away from an aerotactic band when the magnetic field is reversed. In this situation, cells do not encounter the redox condition that switches them into the other state and hence do not reverse their swimming direction. It also accounts for the fact that in the capillary with both ends open NS polar bacteria only form a stable band at the end for which the oxygen gradient and B are anti-parallel. Unlike the axial cells, polar cells have been observed to stop swimming and remain stationary by attachment to a solid surface or other cells at the optimum oxygen concentration, resuming swimming when the oxygen concentration changes. Finally, in some polar strains exposure to light of short wavelengths (= 500 nm) can switch the cell into the "oxidized state" even in reducing conditions for which the oxygen concentration is sub-optimal.

Figure 3 Schematic showing how polar magneto-aerotaxis keeps cells at the preferred oxygen concentration in the oxic-anoxic transition zone (OATZ) in chemically stratified water columns and sediments (NH,Northern hemishpere; SH, Southern hemisphere; Bgeo geomagnetic field). In both hemispheres, cells at higher than optimal oxygen concentration in the ëoxidized stateí swim forward by rotating their flagella counter clockwise (ccw), whereas cells at lower than optimal oxygen concentration in the ërreduced stateí 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.

The polar magneto-aerotaxis model would also apply to SS polar magneto-aerotactic bacteria if it is assumed that their flagellar rotation is also ccw in the "oxidized" state, and cw in the "reduced" state. In flat capillaries with both ends open, SS bacteria would also form only a single band but at the end of the capillary for which the magnetic field is parallel to the oxygen concentration gradient, i.e., at other end from that at which the NS band forms.

When a natural sample of sediment and water containing polar magneto-aerotactic bacteria from a Northern hemisphere habitat was incubated in a magnetic field coil that inverted the vertical component of the local magnetic field, it was found that the ratio of SS cells to NS cells increased with time over several weeks until SS cells predominated. This can be understood in terms of a model in which daughter cells in each generation inherit genes for making magnetosomes, but their polarity (NS or SS) is determined by the magnetosomes inherited from the parent cell during cell division. If the parental magnetosomes are divided between the daughter cells, both cells could inherit the parental polarity. But if some cells did not inherit any parental magnetosomes, they would have a 50% probability of acquiring the opposite polarity as they start making magnetosomes. So in each generation, a minority of SS cells might be expected in a predominantly NS population. Since NS cells are favored in the Northern hemisphere, the average fraction of SS cells in the population remains low. However, when the vertical component of the magnetic field is inverted, the SS cells are favored and they eventually become the majority polarity in the population. This process might also occur in a given location during reversals or excursions of the geomagnetic field. A further indication that cell polarity is not determined genetically comes from the fact that SS cells can result when NS cells are pulsed with magnetic fields greater than the coercive force of the magnetosome chain (ca. 300 gauss), with the magnetic pulse oriented opposite to the local background magnetic field.

It has been suggested that the model of polar magneto-aerotaxis could be extended to a more comples redoxtaxis in habitats in which rapid chemical oxidation of reduced chemical species such as sulfur near the OATZ results in separated pools of reductants and oxidants (Spring and Bazylinski, 2000). For some magnetotactic bacteria, it might be necessary to perform excursions to anoxic zones of their habitat in order to accumulate reduced sulfur compounds. In this situation, polar magnetotaxis could efficiently guide bacteria, either downward to accumulate reduced sulfur species or upward to oxidize stored sulfur with oxygen. The "oxidized state" would result from the almost complete consumption of stored sulfur or another electron donor, and the cells would swim parallel to B toward deeper anoxic layers where they could replenish the depleted stock of electron donor using nitrate or other compounds as alternative electron acceptor. Finally, they would reach a "reduced state" in which the electron acceptor is depleted. In this state the cells would swim anti-parallel to B to return to the micro-oxic zone where oxygen is available to them as an electron acceptor. The advantage of polar magnetotaxis is that an oxygen gradient is not necessary for efficient orientation in the anoxic zone, thereby enabling a rapid return of the cell along large distances to the preferred micro-oxic conditions. A further benefit would be that cells avoid the waste of energy by constant movement along gradients, but instead can attach to particles in preferred micro-niches until they reach an unfavorable internal redox state that triggers a magnetotactic response either parallel or anti-parallel to the geomagnetic field lines. In any case, greater than optimal concentrations of oxygen would switch cells immediately to the "oxidized state" provoking the typical down-seeking response of magnetotactic bacteria under oxic conditions.

4. References
Bazylinski, DA and Frankel, RB (2000) Biologically controlled mineralization of magnetic iron minerals by magnetotactic bacteria. In: . Lovley, DR (ed) Environmental Microbe-Metal Interactions.ASM Press, Washington, D.C.

Blakemore, RP (1982) Magnetotactic bacteria. Annual Reviews of Microbiology 36: 217-238.

Frankel, RB (1984) Magnetic Guidance of Organisms. Annual Review of Biophysics and Bioengineering. 13:85-103.

Frankel, RB, Bazylinski, DA, Johnson, MS and Taylor, BL (1997) Biophysics Journal 73:994-1000.

Gorby, YA, Beveridge, TJ, and Blakemore, RP (1988) characterization of the bacterial magnetotsome membrane. Journal of Bacteriology 170:834-841.

Moskowitz, BM (1995) Biomineralization of magnetic iron minerals. Reviews of Geophysics Supplement 33:1234-128.

Sakaguchi, T, Burgess, JG, and Matunaga, T (1993) Magnetite formation by a sulphate-reducing bacterium. Nature 365:47-49.

Schüler, D, Spring, S, Bazylinski, DA (1999) Improved technique for the isolation of magnetotactic spirilla from freshwater sediment and their phylogenetic characterization. Systemic and Applied Microbiology 22:466-471.

Spring, S, and Bazylinski, DA, (2000) Magnetotactic bacteria. In: The Prokaryotes.
published on the web at, Springer-Verlag, New York.

5. Further Reading
Blakemore, RP and Frankel, RB (1981) Magnetic navigation in bacteria. Scientific American 245(6):58-65.

Dunin-Borkowski, RE, McCartney, M R, Frankel, RB, Bazylinski, DA, Posfai, M, and Buseck, PR (1998) Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282:2868-1870.

Frankel, RB and Blakemore RP (eds) (1991) Iron Biominerals Plenum Press, New York.

Mann, S, Sparks, NHC, and Board, RG (1990) Magnetotactic bacteria: , Microbiology, biomineralization, palaeomagnetism and biotechnology. Advances in Microbial Physiology 31:125-181.

Moench, TT, and Konetzka, WA (1978) A novel method for the isolation and study of a magnetotactic bacterium. Archives of Microbiology 119:203-212.

Sakaguchi, T, Tsujimura, N and Matsunaga T (1996) A novel method for isolation of magnetic bacteria without magnetic collection using magnetotaxis, Journal of Microbiological Methods 26:139-145.

Taylor, BL, Zhulin, IB, and Johnson, MS (1999) Aerotaxis and other energy-sensing behavior in bacteria. Annual Reviews of Microbiology 53:103-128.

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