Magnetotaxis in Prokaryotes

Christopher T Lefèvre, CEA Cadarache, Saint‐Paul‐lez‐Durance, France
Richard B Frankel, California Polytechnic State University, San Luis Obispo, USA
Dennis A Bazylinski, University of Nevada, Las Vegas, USA

Published online: December 2011

DOI: 10.1002/9780470015902.a0000397.pub2

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 location and retention in the cell's preferred habitat 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 by the large number of different morphotypes found in environmental samples of water or sediment, and by phylogenetic analysis of both cultured and uncultured organisms.

Key Concepts:

  • Prokaryotes (bacteria), like eukaryotes, internally compartmentalise and contain organelles.
  • The prokaryotic flagellum rotates clockwise and counter clockwise thereby propelling the cell during swimming.
  • Magnetotaxis is bacterial motility directed by a magnetic field.
  • 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 to increase energy transduction in magnetotactic bacteria.
  • Genes for magnetosome formation are clustered in a region of the genomes of magnetotactic bacteria known as a magnetosome gene or genomic island.
  • 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. Phylogenetic tree, based on 16S receptor ribonucleic acid (rRNA) gene sequences, showing the phylogenetic position of known magnetotactic bacteria (bold) and their closest relatives in the Domain Bacteria. The tree is based on neighbour-joining analyses. Bar represents 2% sequence divergence.
Figure 2. (a) Differential interface contrast (DIC) light micrograph of North-seeking (NS) magnetotactic bacteria, with polar magnetotaxis, aggregated at the edge of the drop of a ‘hanging drop’. (b) Magnetic enrichment of magnetotactic bacteria from an environmental sample by applying the south pole of a magnet (M) several centimeters above the water–sediment interface for 30 min. Magnetotactic bacteria that accumulate at the magnet are shown as a dark spot at the arrow.
Figure 3. Transmission electron micrograph (TEM) images of magnetotactic bacteria and magnetosomes. (a) TEM of a cell of the genus Magnetospirillum species showing the chain of magnetosomes inside 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 4. 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 centre (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.
Figure 5. Schematic showing how polar magneto-aerotaxis keeps cells at the preferred oxygen 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 oxygen concentration in the ‘oxidised state’ swim forward by rotating their flagella counter clockwise (ccw), whereas cells at lower than optimal oxygen 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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 References
    Abreu F, Cantão M, Nicolás M et al. (2011) Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria. ISME Journal 5: 1634–1640.
    Abreu F, Martins JL, Silveira TS et al. (2007) ‘Candidatus Magnetoglobus multicellularis’, a multicellular, magnetotactic prokaryote from a hypersaline environment. International Journal of Systematic and Evolutionary Microbiology 57: 1318–1322.
    Abreu F, Silva KT, Farina M, Keim CN and Lins U (2008) Greigite magnetosome membrane ultrastructure in ‘Candidatus Magnetoglobus multicellularis’. International Microbiology 11: 75–80.
    Bazylinski DA and Frankel RB (2004) Magnetosome formation in prokaryotes. Nature Reviews in Microbiology 2: 217–230.
    book Bazylinski DA and Williams TJ (2007) "Ecophysiology of magnetotactic bacteria". In: Schüler D (ed.) Magnetoreception and Magnetosomes in Bacteria, pp. 37–75. Heidelberg: Springer.
    Bazylinski DA, Dean AJ, Schüler D, Phillips EJP and Lovley DR (2000) N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environmental Microbiology 2: 266–273.
    Bazylinski DA, Dean AJ, Williams TJ et al. (2004) Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Archives of Microbiology 182: 373–387.
    Bazylinski DA, Frankel RB and Jannasch HW (1988) Anaerobic magnetite production by a marine magnetotactic bacterium. Nature 334: 518–519.
    Bazylinski DA, Heywood BR, Mann S and Frankel RB (1993) Fe3O4 and Fe3S4 in a bacterium. Nature 366: 218.
    Bean CP and Livingston JD (1959) Superparamagnetism. Journal of Applied Physics 30: 120S–129S.
    Bellini S (2009a) On a unique behavior of freshwater bacteria. Chinese Journal of Oceanology and Limnology 27: 3–5.
    Bellini S (2009b) Further studies on “magnetosensitive bacteria”. Chinese Journal of Oceanology and Limnology 27: 6–12.
    Blakemore RP (1975) Magnetotactic bacteria. Science 190: 377–379.
    Blakemore RP (1982) Magnetotactic bacteria. Annual Reviews of Microbiology 36: 217–238.
    Blakemore RP, Frankel RB and Kalmijn AJ (1980) South-seeking magnetotactic bacteria in the southern-hemisphere. Nature 286: 384–385.
    Butler RF and Banerjee SK (1975) Theoretical single-domain grain size range in magnetite and titanomagnetite. Journal of Geophysical Research 80: 4049–4058.
    Dunin-Borkowski RE, McCartney MR, Frankel RB et al. (1998) Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282: 1868–1870.
    Flies CB, Jonkers HM, de Beer D et al. (2005) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiology Ecology 52: 185–195.
    Frankel RB (1984) Magnetic guidance of organisms. Annual Review of Biophysics and Bioengineering 13: 85–103.
    Frankel RB and Bazylinski DA (2006) How magnetotactic bacteria make magnetosomes queue up. Trends in Microbiology 14: 329–331.
    Frankel RB, Bazylinski DA, Johnson MS and Taylor BL (1997) Magneto-aerotaxis in marine, coccoid bacteria. Biophysical Journal 73: 994–1000.
    Frankel RB, Blakemore RP, Torres de Araujo FF et al. (1981) Magnetotactic bacteria at the geomagnetic equator. Science 212: 1269–1270.
    Geelhoed JS, Kleerebezem R, Sorokin DY, Stams AJM and van Loosdrecht MCM (2010) Reduced inorganic sulfur oxidation supports autotrophic and mixotrophic growth of Magnetspirillum strain J10 and Magnetospirillum gryphiswaldense. Environmental Microbiology 12: 1031–1040.
    Gorby YA, Beveridge TJ and Blakemore RP (1988) Characterization of the bacterial magnetotsome membrane. Journal of Bacteriology 170: 834–841.
    Grünberg K, Wawer C, Tebo BM and Schüler D (2001) A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Applied and Environmental Microbiology 67: 4573–4582.
    Hanzlik M, Winklhofer M and Petersen N (2002) Pulsed-field-remanence measurements on individual magnetotactic bacteria. Journal of Magnetism and Magnetic Materials 248: 258–267.
    Heywood BR, Bazylinski DA, Garratt-Reed AJ, Mann S and Frankel RB (1990) Controlled biosynthesis of greigite (Fe3S4) in magnetotactic bacteria. Naturwissenschaften 77: 536–538.
    Jogler C and Schüler D (2009) Genomics, genetics, and cell biology of magnetosome formation. Annual Review of Microbiology 63: 501–521.
    Jogler C, Wanner G, Kolinko S et al. (2011) Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proceedings of the National Academy of Sciences of the USA 108: 1134–1139.
    Komeili A, Li Z, Newman DK and Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311: 242–245.
    Komeili A (2007) Molecular mechanisms of magnetosome formation. Annual Reviews of Biochemistry 76: 351–366.
    Lefèvre C, Bernadac A, Pradel N et al. (2007) Characterization of Mediterranean magnetotactic bacteria. Journal of Ocean University of China 6: 355–359.
    Lefèvre CT, Abreu F, Lins U and Bazylinski DA (2010a) Non-magnetotactic multicellular prokaryotes from low saline, nonmarine aquatic environments and their unusual negative phototactic behavior. Applied and Environmental Microbiology 76: 3220–3227.
    Lefèvre CT, Abreu F, Schmidt ML et al. (2010b) Moderately thermophilic magnetotactic bacteria from hot springs in Nevada. Applied and Environmental Microbiology 76: 3740–3743.
    Lefèvre CT, Bernadac A, Song T et al. (2009a) Characterization of a novel axenic magnetotactic bacterial culture isolated from the Mediterranean Sea. Environmental Microbiology 11: 1646–1657.
    Lefèvre CT, Frankel RB, Abreu F, Lins U and Bazylinski DA (2011a) Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environmental Microbiology 13: 538–549.
    Lefèvre CT, Frankel RB, Pósfai M, Prozorov T and Bazylinski DA (2011b) Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environmental Microbiology 13: 2342–2350.
    Lefèvre CT, Song T, Yonnet JP and Wu LF (2009b) Characterization of bacterial magnetotactic behaviors by using a magnetospectrophotometry assay. Applied and Environmental Microbiology 75: 3835–3841.
    Lefèvre CT, Viloria N, Pósfai M, Frankel RB and Bazylinski DA (2011c) Novel magnetite-producing magnetotactic bacteria phylogenetically affiliated with the Gammaproteobacteria class. ISME Journal. doi: 10.1038/ismej.2011.97.
    Lin W, Jogler C, Schüler D and Pan Y (2011) Metagenomic analysis reveals unexpected subgenomic diversity of magnetotactic bacteria within the phylum Nitrospirae. Applied and Environmental Microbiology 77: 323–326.
    Lins U, Freitas F, Keim CN et al. (2003) Simple homemade apparatus for harvesting uncultured magnetotactic Microorganisms. Journal of Microbiology 34: 111–116.
    Lins U, Keim CN, Evans FF, Buseck PR and Farina M (2007) Magnetite (Fe3O4) and greigite (Fe3S4) crystals in multicellular magnetotactic prokaryotes. Geomicrobiology Journal 24: 43–50.
    Mann S, Frankel RB and Blakemore RP (1984) Structure, morphology and crystal growth of bacterial magnetite. Nature 310: 405–407.
    Mann S, Sparks NHC, Frankel RB, Bazylinski DA and Jannasch HW (1990) Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343: 258–260.
    Maratea D and Blakemore RP (1981) Aquaspirillum magnetotacticum sp. nov., a magnetic spirillum. International Journal of Systematic Bacteriology 31: 452–455.
    Matsunaga T, Sakaguchi T and Tadokoro F (1991) Magnetite formation by a magnetic bacterium capable of growing aerobically. Applied Microbiology and Biotechnology 35: 651–655.
    Meldrum FC, Heywood BR, Mann S, Frankel RB and Bazylinski DA (1993) Electron microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium. Proceedings of the Royal Society of London Series B-Biological Sciences 251: 231–236.
    Moskowitz BM, Bazylinski DA, Egli R, Frankel RB and Edwards KJ (2008) Magnetic properties of marine magnetotactic bacteria in a seasonally stratified coastal pond (Salt Pond, MA, USA). Geophysical Journal International 174: 75–92.
    Moskowitz BM, Frankel RB, Flanders PJ, Blakemore RP and Schwartz BB (1988) Magnetic properties of magnetotactic bacteria. Journal of Magnetism and Magnetic Materials 73: 273–288.
    Murat D, Quinlan A, Vali H and Komeili A (2010) Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proceedings of the National Academy of Sciences of the USA 107: 5593–5598.
    Penninga I, de Waard H, Moskowitz BM, Bazylinski DA and Frankel RB (1995) Remanence measurements on individual magnetotactic bacteria using pulsed magnetic fields. Journal of Magnetism and Magnetic Materials 149: 279–286.
    Pósfai M, Buseck PR, Bazylinski DA and Frankel RB (1998a) Reaction sequence of iron sulphide minerals in bacteria and their use as biomarkers. Science 280: 880–883.
    Pósfai M, Buseck PR, Bazylinski DA and Frankel RB (1998b) Iron sulfides from magnetotactic bacteria: structure, composition, and phase transitions. American Mineralogist 83: 1469–1481.
    Pradel N, Santini CL, Bernadac A, Fukumori Y and Wu LF (2006) Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proceedings of the National Academy of Sciences of the USA 103: 17485–17489.
    Sakaguchi T, Arakaki A and Matsunaga T (2002) Desulfovibrio magneticus sp. nov., a novel sulfate reducing bacterium that produces intracellular single-domain-sized magnetite particles. International Journal of Systematic and Evolutionary Microbiology 52: 215–221.
    Sakaguchi T, Burgess JG and Matsunaga T (1993) Magnetite formation by a sulphate-reducing bacterium. Nature 365: 47–49.
    Scheffel A, Gruska M, Faivre D et al. (2006) An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440: 110–114.
    Schleifer KH, Schuler D, Spring S et al. (1991) The genus Magnetospirillum gen. nov. description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. Systematic and Applied Microbiology 14: 379–385.
    Schübbe S, Kube M, Scheffel A et al. (2003) Characterization of a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. Journal of Bacteriology 185: 5779–5790.
    Schübbe S, Williams TJ, Xie G et al. (2009) Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Applied and Environmental Microbiology 75: 4835–4852.
    Schüler D (2002) The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. International Microbiology 5: 209–214.
    Schüler D (2008) Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiology Review 32: 654–672.
    book Schüler D (ed.) (2006) Magnetoreception and Magnetosomes in Bacteria. Heidelberg: Springer.
    Simmons SL and Edwards KJ (2007) Unexpected diversity in populations of the many-celled magnetotactic prokaryote. Environmental Microbiology 9: 206–215.
    Simmons SL, Bazylinski DA and Edwards KJ (2006) South seeking magnetotactic bacteria in the northern hemisphere. Science 311: 371–374.
    Simmons SL, Sievert SM, Frankel RB, Bazylinski DA and Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Applied and Environmental Microbiology 70: 6230–6239.
    Spormann AM and Wolfe RS (1984) Chemotactic, magnetotactic and tactile behaviour in a magnetic spirillum. FEMS Microbiology Letters 22: 171–177.
    Spring S, Amann R, Ludwig W et al. (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Applied and Environmental Microbiology 59: 2397–2403.
    Ullrich S, Kube M, Schübbe M, Reinhardt R and Schüler D (2005) A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. Journal of Bacteriology 187: 7176–7184.
    Williams TJ, Zhang CL, Scott JH and Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Applied and Environmental Microbiology 72: 1322–1329.
    Zhao L, Wu D, Wu LF and Song T (2007) A simple and accurate method for quantification of magnetosomes in magnetotactic bacteria by common spectrophotometer. Journal of Biochemical and Biophysical Methods 70: 377–383.
    Zhu K, Pan H, Li J et al. (2010) Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Research in Microbiology 161: 276–283.
 Further Reading
    Bazylinski DA and Schübbe S (2007) Controlled biomineralization by and applications of magnetotactic bacteria. Advances in Applied Microbiology 62: 21–62.
    Frankel RB and Bazylinski DA (2009) Magnetosomes and magneto-aerotaxis. Contribution in Microbiology 16: 182–193.
    Moskowitz BM (1995) Biomineralization of magnetic iron minerals. Reviews of Geophysics Supplement 33: 1234–1128.
    book Schüler D (ed.) (2007) Microbiological Monographs Vol. 3: Magnetoreception and Magnetosomes in Bacteria, pp. 319 Berlin, Heidelberg: Springer-Verlag.
    Taylor BL, Zhulin IB and Johnson MS (1999) Aerotaxis and other energy-sensing behavior in bacteria. Annual Reviews of Microbiology 53: 103–128.

Related Sub-Topics:

Cell Compartments and Cellular Organelles | Cell Motility | Cell Motility and Transport | Optical Microscopy | Composition and Structure of Microbial Cells | Bacteria
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Article Title: Magnetotaxis in Prokaryotes
 
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Lefèvre, Christopher T, Frankel, Richard B, and Bazylinski, Dennis A(Dec 2011) Magnetotaxis in Prokaryotes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000397.pub2]