MAGNETOTACTIC BACTERIA
AT CAL POLY
Department
of Physics, Cal Poly State University, San Luis Obispo, CA 93407
E – mail: rfrankel@calpoly.edu
Magnetotactic
bacterium strain MV-1 Magnetotactic behavior in
bacteria was discovered over 20 years ago [1]. The discovery was based on the
fact that microscopic examination of a drop of water and sediment from a pond,
lake or marsh on a microscope slide in a magnetic field of a few gauss
(comparable in strength to the geomagnetic field) can reveal bacteria migrating
persistently along magnetic field lines in the field direction, corresponding
to Northward migration along geomagnetic field lines [3]. The migration speed
of individual bacteria along the magnetic field lines depends on the field
strength, but can be 90% or more of the forward swimming speed (up to 150
microns per second) of the cell. If the direction of the local magnetic field
is reversed, the magnetotactic bacteria execute "U-turns" and
continue migrating in the same direction relative to the local magnetic field.
The migration direction of bacteria in the magnetic field can be reversed by
subjecting the cells to a strong (several hundred gauss) magnetic field pulse
oriented opposite to the field in which they are migrating [4]. Magnetotactic
bacteria that spontaneously migrate Southward along geomagnetic field lines are
found in aquatic sediments and waters from the Southern Hemisphere [5]. Reviews
of recent research on magnetotactic bacteria may be found in reference [6].
Magnetosome
mineral particles
All magnetotactic bacteria contain magnetosomes [7], which are magnetic mineral particles enclosed in membranes. In most cases the magnetosomes are arranged in a chain or chains [2], apparently fixed within the cell. In many magnetotactic bacterial types, the magnetosome mineral particles are magnetite, Fe3O4 [8-12], and are characterized by a narrow size distribution, and uniform, species-specific, crystal habits [13, 14]. The particle sizes range from ca. 40 to 100 nm, which are within the permanent single-magnetic-domain size range for magnetite.
In magnetotactic bacteria
from marine, sulfidic environments, the magnetosome particles are the
iron-sufide mineral greigite, Fe3S4, [15-18], which is
isostructural with magnetite and is also ferrimagnetically ordered at ambient
temperature. The greigite particles are also characterized by a narrow size
distribution and species-specific crystal habits. However, whereas the
magnetite particles in a magnetosome chain are usually oriented so that a [111]
crystallographic axis of each particle lies along the chain direction, the
greigite particles in a magnetosome chain are usually oriented so that a [100]
crystallographic axis of each particle is oriented along the chain direction
[17].
Cellular magnetic
dipole
Whether the mineral particles are magnetite or greigite, the chain of magnetosome particles constitutes a permanent magnetic dipole fixed within the bacterium [3]. The magnetic dipole moment is generally sufficiently large so that it, and consequently the bacterium, is oriented in the geomagnetic field so that <cosØ> 0.9, where Ø is the instantaneous angle between the magnetic dipole moment and the field direction. Magnetotaxis is a passive process in which the orientation of the magnetic dipole in the ambient magnetic field as the organism swims causes it to migrate along the magnetic field lines.
Magnetotactic bacteria have two
possible magnetic polarities, depending on the orientation of the magnetic
dipole within the cell. The polarity can be reversed by a magnetic pulse which
is greater than the coercive force of the chain of particles. As noted above,
bacteria with reversed polarity migrate along magnetic field lines in the
direction opposite to that of bacteria with the original polarity. In natural
habitats, the predominant polarity type in the population of a given bacterial
species is determined by the sign of the inclination of the geomagnetic field
[5].
Chemically
stratified sites
It has recently been
reported that high concentrations of bacteria occur in a horizontal
"plate" at the oxic-anoxic transition zone (OATZ) in stratified
marine environments [19]. In these environments, downward oxygen diffusion from
the surface and upward sulfide diffusion, resulting from bacterial sulfate
reduction in the anaerobic sediment, create a double vertical chemical
concentration gradient system, with a concomitent redox gradient. In the
Pettaquamscutt Estuary in Narragansett Bay, Rhode Island, the OATZ occurs at
about 4.5 meters in a 20 meter water column, and the bacterial concentration in
the plate is greater than 106 cells per cc. At least seven
morphologically-distinct, magnetotactic-bacterial types occur at the OATZ
[20-21], some containing Fe3O4 particles, and some
containing Fe3O4 particles [21]. The magnetite-containing
cells tend to be more abundant at the top of the plate, in the relatively
oxygen-rich portion of the OATZ, while the greigite-containing cells tend to be
more abundant at the bottom of the plate, in the relatively sulfide-rich
portion of the OATZ.
Papers on magnetotatic
bacteria by Richard B. Frankel
Additional papers on
magnetotatic bacteria
References
1.
R. P. Blakemore, Science 190, (1975) 377.
2. R.P. Blakemore, N.A. Blakemore, D.A. Bazylinski, and T.T Moench, in: Bergey's Manual of Systematic Bacterioloqy Vol. 3, eds. M. P. Bryant, N. Pfennig, and J. T. Staley, (Williams and Wilkins, Baltimore, 1989) 1882.
3. R. B. Frankel, Ann. Rev. Biophys. Bioeng. 13, (1984) 85.
4. A. J. Kalmijn and R. P. Blakemore, in: Animal Migration and Homing, eds. K. Schmidt-Koenig and W. T. Keeton (Springer Verlag, New York, 1978) 344.
5. R. P. Blakemore, R. B. Frankel and A. J. Kalmijn, Nature 286, (1980) 384.
6. R. B. Frankel and R. P. Blakemore, Eds. Iron Biominerals (Plenum Press, New York, 1990).
7. D. L. Balkwill, D. Maratea, and R. P. Blakemore, J. Bacteriol. 141, (1980) 1399.
8. R. B. Frankel, R. P. Blakemore, and R. S. Wolfe, Science 203, (1979) 1355.
9. K. M. Towe, and T. T. Moench, Earth Planet. Sci. Lett. 52, (1981) 213.
10. T. Matsuda, J. Endo, N. Osakabe, A. Tonomura, A. and T. Arii, Nature 343, (1983) 258.
11. S. Mann, N. H. C. Sparks, and R. P. Blakemore, Proc. Roy. Soc. Lond. B 231, (1987) 469.
12. D. A. Bazylinski, R. B. Frankel, R.B. and H. W. Jannasch, H.W. Nature 334, (1988) 518.
13. F. C. Meldrum, B. R. Heywood, S. Mann, R. B. Frankel, and D. A. Bazylinski, Proc. Roy. Soc. Lond. B 251, (1993) 231; Proc. Roy. Soc. Lond. B 251, (1993) 237.
14. S. Mann, and R. B. Frankel, in: Biomineralization: Chemical and Biological Perspectives, eds. S. Mann, J. Webb, and R. J. P. Williams (Springer Verlag, Berlin, 1990) pp. 389-426.
15. S. Mann, N. H. C. Sparks, R. B. Frankel, D. A. Bazylinski, and H. W. Jannasch, Nature 343, (1990) 258.
16. B. R. Heywood, D. A. Bazylinski, A. J. Garratt-Reed, S. Mann, and R. B. Frankel, Naturwissenschaften 77, (1991) 536.
17. B. R. Heywood, S. Mann, and R. B. Frankel, in: Materials Synthesis Based on Biological Processes, eds. M. Alpert, et al. (Materials Research Society, Pittsburgh, PA, 1990) 93.
18. M. Farina, D. M. S. Esquivel, and H. G. P. Lins de Barros, Nature 334, (1990) 256.
19. P. L. Donaghay, H. M. Rines, and J. McN. Sieburth, Arch. Hydrobiol. Beih. Ergebn. Limnol. 36, (1992) 96.
20. Stolz, J.F. in Biomineralization Processes of Iron and Manqanese-Modern and Ancient Environments, eds. H. W. C. Skinner, and R. W. Fitzpatrick (Catena Verlag, Cremlingen-Destedt, 1992) 133.
21. D. A. Bazylinski, R. B. Frankel, B. R. Heywood, S. Mann, J. King, P.L. Donaghay, and A.K. Hanson, Appl. Environ. Microbiol. 61, (1995) 3232.
Publications
on Magnetotatic Bacteria by Richard B. Frankel and Collaborators
(A=abstract; R=review)
1.
R.B.
Frankel, R.P. Blakemore, and R.S. Wolfe: Magnetite in Freshwater Magnetic
Bacteria. Science 203, 1355-1357 (1979).
2.
C.R.
Denham, R.P. Blakemore, and R.B. Frankel: Bulk Magnetic Properties of
Magnetotactic Bacteria. IEEE Trans. Magn. MAG-16, 1006-1007 (1980).
3.
R.B.
Frankel and R.P. Blakemore: Navigational Compass in Magnetic Bacteria. J. Magn.
and Magn. Mater. 15-18, 1562-1564 (1980).
4.
R.P.
Blakemore, R.B. Frankel and Ad.J. Kalmijn: South-seeking Magnetotactic Bacteria
in the Southern Hemisphere. Nature (London) 236, 384-385 (1980).
5.
R.B.
Frankel: Bacterial Magnetotaxis vs Geotaxis. Trans. Am. Geophys. Soc. (EOS) 62,
850 (1981). A
6.
R.B.
Frankel, R.P. Blakemore, F.F. Torres de Araujo, D.M.S.Esquivel, and J. Danon:
Magnetotactic Bacteria at the Geomagnetic Equator.Science 212, 1269-1270
(1981).
7.
R.
P. Blakemore and R. B. Frankel: Magnetic Navigation in Bacteria.
Scientific American 245, Vol. 6, 58-65 (1981). R
8.
C.
Rosenblatt, F. F. Torres de Araujo, and R.B. Frankel: Birefringence
Determination of Magnetic Moments of Magnetotactic Bacteria. Biophys. J. 40,
83-85 (1982).
9.
C.
Rosenblatt, F.F. Torres de Araujo, and R.B. Frankel: Light Scattering
Determination of Magnetic Moments of Magnetotactic Bacteria. J. Appl. Phys. 53,
2727-2729 (1982).
10.
R.B.
Frankel: Magnetotactic Bacteria. Comments Mol. Cell. Biophys. 1, 293-310
(1982). R
11.
R.B.
Frankel, G.G. Papaefthymiou, R.P. Blakemore, and W. O'Brien:
Fe3O4 Precipitation in Magnetotactic Bacteria. Biochim.
Biophys. Acta 763, 147-159 (1983).
12.
R.B.
Frankel and G.C. Papaefthymiou: Biomineralization of Fe3O4 in Bacteria.
Chemical Mössbauer Spectroscopy, Ed: R.H. Herber, (Plenum Press, NY,
1984), pp. 113-132. R
13.
R.B.
Frankel: Magnetic Guidance of Organisms. Ann. Rev. Biophys. Bioengr. 13, 85-103
(1984). R
14.
S.
Ofer, I. Nowik, E.R. Bauminger, G.C. Papaefthymiou, R.B. Frankel and R.P.
Blakemore:
Magnetosome Dynamics in Magnetotactic Bacteria. Biophys. J. 46, 57-64 (1984).
15.
R.B.
Frankel and R.P. Blakemore: Precipitation of Fe3O4 in Magnetotactic Bacteria.
Trans. Roy. Soc. Lond. B304, 567-574 (1984). R
16.
S.
Mann, R.B. Frankel, and R.P. Blakemore: Structure, Morphology, and Crystal
Growth of Bacterial Magnetite. Nature 310, 405-407 (1984).
17.
C.
Rosenblatt, R.B. Frankel, and R.P. Blakemore: A Birefringence Relaxation
Determination of Rotational Diffusion of Magnetotactic Bacteria. Biophys. J.
47, 323-325 (1985).
18.
R.P.
Blakemore, R.A. Short, C. Bazylinski, C. Rosenblatt, and R.B. Frankel:
Microaerobic Conditions are Required for Magnetite Formation Within
Aquaspirillum Magnetotacticum. Geomicrobiology J. 4, 53-71 (1985).
19.
R.B.
Frankel, G.C. Papaefthymiou, and R.P. Blakemore: Mössbauer Spectroscipy of
Iron Biomineralization Products in Magnetotactic Bacteria. in: Magnetite
Biomineralization and
Magnetoreception in Organisms, J.L. Kirschvink, D.S. Jones, and B.J. MacFadden,
Editors.
(Plenum, NY, 1985), pp. 269-287 R
20.
F.F.
Torres de Araujo, M.A. Pires, R.B. Frankel, and C.E.M. Bicudo: Magnetite and
Magnetotaxis in Algae. Biophys. J. 50, 375-378 (1986).
21.
R.B.
Frankel: Magnetite and Magnetotaxis in Bacteria and Algae. Biophysical Effects
of Steady Magnetic Fields, edited by G. Maret (Springer-Verlag, Berlin, 1986)
pp. 173-179. R
22.
R.P.
Blakemore, N.A. Blakemore, and R.B. Frankel: Bacterial Biomagnetism and
Geomagnetic Field Detection by Organisms. Modern Bioelectrcity, edited by A.A.
Marino,
(Dekker, NY, 1988), pp. 19-29. R
23.
B.M.
Moskowitz, R.B. Frankel, P. Flanders, R.P. Blakemore and B.B. Schwartz:
Magnetic Properties of Magnetotactic Bacteria. J. Magn. and Magn. Mater. 73,
273-288 (1988).
24.
R.B.
Frankel and R.P. Blakemore: Magnetite and Magnetotaxis in Microorganisms.
Biotechnological Applications of Lipid Microstructures, Editors: B. Gaber, J.
Schnur and D Chapman. (Plenum Press, New York, 1988) pp.321-330. R
25.
D.A.
Bazylinski, R.B. Frankel, and H.W. Jannasch: Anaerobic Magnetite Production by
a Marine, Magnetotactic Bacterium. Nature 334, 518-519 (1988).
26.
S.
Mann and R.B. Frankel: Magnetite Biomineralization in Unicellular Organisms.
Biomineralization: Chemical and Biochemical Perspectives, Editors:S. Mann, J.
Webb and
R.J.P. Williams.(CVH Press, Mannheim, FRG, 1989) pp.389-426. R
27.
D.
Guell, H. Brenner, R.B. Frankel, and H. Hartman: Hydrodynamic Forces and Band
Formation in Swimming Magnetotactic Bacteria. J. Theor. Biol. 135, 525-542
(1989).
28.
R.B.
Frankel and R.P. Blakemore: Magnetite and Magnetotaxis in Bacteria.
Bioelectromagnetics 10, 223-237 (1989). R
29.
R.P.
Blakemore and R.B. Frankel: Biomineralization by Magnetogenic Bacteria.
Metal-Microbe Interactions, Edited by R.K.Poole and G.M.Gadd (IRL Press,
Oxford, UK, 1989) pp.85-98. R
30.
B.M.
Moskowitz, R.B. Frankel, D.A. Bazylinski, and D.R. Lovley: Comparison of
Magnetic Properties of Magnetite Produced by Anaerobic Magnetotactic and
Dissimilatory Iron Reducing Bacteria. Geophys. Res. Letters 16, 665-668 (1989).
31.
N.H.C.
Sparks, S. Mann, D. Bazylinski, D.R. Lovley, H.W. Jannasch and R.B. Frankel:
Structure and Morphology of Magnetite Anaerobically-Produced by a Marine
Magnetotactic Bacterium and a Dissimilatory Iron-reducing Bacterium. Earth
& Planet. Sci. Lett. 98, 14-22 (1990).
32.
F.F.
Torres de Araujo, N.A. Germano, L.L. Goncalves, M.A. Pires and R.B. Frankel:
Magnetic Polarity Fractions in Magnetotactic Bacterial Populations Near the
Geomagnetic Equator. Biophys. J. 58, 549 (1990).
33.
S.
Mann, N.H.C. Sparks, R.B. Frankel, D.A. Bazylinski and H.W. Jannasch:
Biomineralization of Ferrimagnetic Greigite (Fe3S4) and
Iron Pyrite (FeS2) in a Magnetotactic Bacterium. Nature 343, 258-261
(1990).
34.
F.G.
Rodgers, R.P. Blakemore, N. Blakemore, R.B. Frankel, D.A. Bazylinski, D.
Maratea, C. Rodgers: Intercellular Connections in a Many-Celled Magnetotactic
Prokaryote. Arch. Microbiol. 154, 18-22 (1990).
35.
B.R.
Heywood, D.A. Bazylinski, A.J. Garratt-Reed, S. Mann, and R.B. Frankel:
Controlled Biosynthesis of Greigite in Magnetotactic Bacteria.
Naturwissenschaften 77, 536-538 (1990).
36.
R.B.
Frankel and R.P. Blakemore, Editors: Iron Biominerals, Plenum Press, New York,
1991, 435 pages.
37.
R.
B. Frankel: Iron Biominerals: An Overview. In: Iron Biominerals, edited by R.B.
Frankel and R.P. Blakemore (Plenum
Press, N.Y., 1991) pp.1-6. R
38.
D.A.
Bazylinski, R.B. Frankel, A. Garratt-Reed, and S. Mann: Biomineralization of
Iron Sulfides in Magnetotactic Bacteria from Sulfidic Environments. In: Iron
Biominerals, edited by R.B.Frankel and R.P. Blakemore (Plenum Press, N.Y.,
1991) pp.239-255. R
39.
R.B.
Frankel: Inorganic Particles Produced by Microorganisms. In: Materials
Syntheses Based on Biological Processes, Vol. 218, edited by M. Alpert et al.
(Materials Research Society, Pittsburgh, PA, 1991) pp.77-79. R
40.
B.R.
Heywood, S. Mann, and R.B. Frankel:Structure, Morphology and Growth of Biogenic
Greigite (Fe3S4). In: Materials Syntheses Based on
Biological Processes, Vol. 218, edited by M. Alpert et al. (Materials Research
Society, Pittsburgh, PA, 1991) pp.93-108.
41.
D.P.E.
Dickson and R.B. Frankel: Magnetic Fine Particles in Biological Systems. In:
Studies of Magnetic Properties of Fine Particles and Their Relevance to
Materials Science, edited by J.L.Dormann and D. Fiorani, (Elsevier, Amsterdam,
1992) pp. 393-402. R
42.
E.F.
DeLong, R.B. Frankel, and D.A. Bazylinski: Multiple Evolutionary Origins of
Magnetotaxis in Bacteria. Science 259, 803-806 (1993).
43.
D.A.
Bazylinski and R.B. Frankel: Production of Iron Sulfide Minerals by
Magnetotactic Bacteria in Sulfidic Environments. In: Biological and
Mineralogical Processes of Fe and Mn
Precipitation in Contemporary Environments, edited by R. Fitzpatrick and H.C.W.
Skinner
(Catena Press, 1993) p.147-159. R
44.
F.C.
Meldrum, S. Mann, B.R. Heywood, R.B. Frankel, and D.A. Bazylinski: Electron
Microscope Study of Magnetosomes in a Cultured Coccoid Magnetotactic Bacterium.
Proc. Roy. Soc. B 251, 231-236 (1993).
45.
F.C.
Meldrum, S. Mann, B.R. Heywood, R.B. Frankel, and D.A. Bazylinski: Electron
Microscope Study of Magnetosomes in Two Cultured Vibrioid Magnetotactic
Bacteria.
Proc. Roy. Soc. B 251, 237-242 (1993).
46.
D.A.
Bazylinski, A.J. Garratt-Reed, A. Abedi and R.B. Frankel: Copper Association
with Iron-Sulfide Magnetosomes in a Magnetotactic Bacterium. Arch. Microbiol.,
160, 35-42 (1993).
47.
D.A.
Bazylinski, B.R. Heywood, S. Mann and R.B. Frankel: Fe3O4
and Fe3S4 in a Bacterium. Nature 366, 218 (1993).
48.
B.M.
Moskowitz, R.B. Frankel, and D.A. Bazylinski: Rock Magnetic Criteria for the
Detection of Biogenic Magnetite. Earth Planet. Sci. Lett. 120, 283-300 (1993).
49.
D.A.
Bazylinski, A.J. Garratt-Reed, and R.B. Frankel: Electron Microscope Studies of
Magnetosomes in Magnetotactic Bacteria. Microsc. Res. Tech. 27, 389-401 (1994).
50.
R.B.
Frankel and D.A. Bazylinski: Magnetotaxis and Magnetic Particles in Bacteria.
Hyperfine Interactions 90, 135-142 (1994).
51.
R.B.
Frankel and D.A. Bazylinski: Structure and Function of Magnetosomes in
Magnetotactic Bacteria. In: Design and Processing of Materials by Biomimetics,
edited by M. Sarikaya and I. Aksay (AIP Press, New York, 1995) pp. 199-216. R
52.
R.B.
Proksch, B.M. Moskowitz, E.D. Dahlberg, T. Schaeffer, D.A. Bazylinski, and R.B.
Frankel:
Magnetic Force Microscopy of the Submicron Magnetic Assembly in a Magnetotactic
Bacterium. Applied Phys. Lett. 66, 2582-2584 (1995).
53.
E.D.
Dahlberg, R.B. Proksch, B.M. Moskowitz, D.A. Bazylinski,and R.B.
Frankel:Microbes, Magnetism and Microscopy. J. Magn. Magn. Mater. 140-144,
1459-1461 (1995).
54.
D.A.
Bazylinski, R.B. Frankel, B.R. Heywood, S. Mann, J.W. King, P.L. Donaghay, and
A.K. Hanson: Controlled Biomineralization of Magnetite (Fe3O4)
and Greigite (Fe3S4) in a Magnetotactic Bacterium.
Applied Environ. Microbiol. 61, 3232-3239 (1995).
55.
Penninga,
H. de Waard, B. Moskowitz, D.A. Bazylinski,and R.B. Frankel:Remanence
Measurements on Individual Magnetotactic BacteriaUsing Pulsed Magnetic Fields.
J. Magn. Magn. Mater. 149, 279-286 (1995).
56.
R.B.
Frankel, D.A. Bazylinski, M. Johnson and B.L. Taylor:Magneto-aerotaxis in Marine,
Coccoid, Bacteria. Biophys. J. 73, 994-1000 (1997).
57.
M.
Posfai, P.R. Buseck, D.A. Bazylinski, and R.B. Frankel: Reaction Sequence of
Iron Sulfide Minerals in Bacteria and Their Use as Biomarkers. Science 280,
880-883 (1998).
58.
M.
Posfai, P.R. Buseck, D. A. Bazylinski, and R.B. Frankel: Iron Sulfides from
Magnetotactic Bacteria: Structure, Composition, and Phase Transitions.:
American Mineralogist 83, 1469-1482 (1998).
59.
B.
Devouard, M. Posfai, X. Hua, D.A. Bazylinski, R.B. Frankel, and P.R. Buseck:
Magnetite from Magnetotactic Bacteria: Size Distributions and Twinning.
American Mineralogist 83, 1387-1399 (1998).
60.
R.B.
Frankel, J-P. Zhang, and D.A. Bazylinski: Single Magnetic Domains in
Magnetotactic Bacteria. Journal of Geophysical Research (Solid Earth) 103,
30601-30604 (1998).
61.
R.B.
Frankel, D.A. Bazylinski and D. Schueler:
Biomineralization of Magnetic Iron Minerals in Bacteria. Supramolecular
Science 5, 383-390 (1998).
62.
R.E.
Dunin-Borkowski, M.R. McCartney, R.B. Frankel, D.A. Bazylinski, M. Posfai and
P.R. Buseck: Magnetic Microstructure of Magnetotactic Bacteria by Electron
Holography. Science 282, 1868-1870 (1998).
63.
D.
Schueler, R. B. Frankel, Bacterial magnetosomes: microbiology,
biomineralization and biotechnological applications. Applied Microbiology and
Biotechnology 52, 464-473 (1999). R
Other
Publications on Magnetotactic Bacteria:
(Note: not a
complete list. See also publications by R.B. Frankel)
1975-1980:
1. R. P. Blakemore, Magnetotactic Bacteria. Science 190, 377-379 (1975).
2. T.T. Moench and W.A. Konetzka, A Novel Method for the Isolation and Study of a Magnetotactic Bacterium. Arch. Microbiol. 119, 203-212 (1978).
3.
J.
Kalmijn and R. P. Blakemore, The Behavior of Mud Bacteria. in: «Animal
Migration and
Homing», eds. K. Schmidt-Koenig, W. T. Keeton
(Springer Verlag, New York, 1978) 344-345.
4.
R.P.
Blakemore, D. Maratea and R.S. Wolfe, Isolation and Pure Culture of a
Freshwater Magnetic Spirillum in Chemically Defined Medium. J. Bacteriol. 140,
720-729 (1979).
5.
L.
Balkwill, D. Maratea, and R. P. Blakemore, Ultrastructure of a Magnetotactic
Spirillum,
J. Bacteriol. 141, 1399-1408 (1980).
6.
J.L.
Kirschvink, South-Seeking Magnetic Bacteria. J. Exp. Biol. 86, 345-347 (1980).
1981-1985:
1.
K.
M. Towe, and T. T. Moench, Electron-Optical Characterization of Bacterial
Magnetite.
Earth Planet. Sci. Lett. 52, 213-220 (1981)
2.
A.J.
Kalmijn, Biophysics of Geomagnetic Field Detection. IEEE Trans. Magn. MAG-17,
1113-1124 (1981)
3.
R.P.
Blakemore, Magnetotactic Bacteria. Ann. Rev. Microbiol. 36, 217-238 (1982).
4.
T.
Matsuda, J. Endo, N. Osakabe, A. Tonomura, A. and T. Arii, Morphology and
Structure of Biogenic Magnetite. Nature 303, 411-412 (1983).
5.
M.
Farina, H. Lins de Barros, D. Esquivel, and J. Danon, Ultrastructure of a
Magnetotactic Bacterium. Biol. Cell 48, 85-88 (1983).
6.
A. Spormann and R.S. Wolfe, Chemotactic, Magnetotactic,
and Tactile Behavior in a Magnetic Spirillum, FEMS Microbiol. Lett. 22, 171-177
(1984).
7.
J.L.
Kirschvink, D.S. Jones, B.J. MacFadden (eds), «Magnetite Biomineralization and
Magnetoreception in Organisms: a New Biomagnetism», (Plenum Press, New York,
1985) 682 pp.
1986-1990:
1.
N.
Petersen, T. Von Dobeneck, and H. Vali, Fossil Bacterial Magnetite in Deep-Sea
Sediments from the South Atlantic. Nature 320, 611-615 (1986).
2.
J.F.
Stoltz, B.R. Chang, and J.L. Kirschvink, Magnetotactic Bacteria and Single
Domain Magnetite in Hemiplagaic Sediments. Nature 321, 849-851 (1986).
3.
S.
Mann, N. H. C. Sparks, and R. P. Blakemore, Ultrastructure and Characterization
of Anisotropic Inclusions in Magnetotactic Bacteria. Proc. Roy. Soc. Lond. B
231, 469-476 (1987).
4.
Y.A.
Gorby, T.J. Beveridge, and R.P. Blakemore, Characterization of the Bacterial
Magnetosome Membrane. J. Bacteriol. 170, 834-841 (1987).
5.
R.P.
Blakemore, N.A. Blakemore, D.A. Bazylinski, and T.T Moench, Magnetotactic
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