Advertisement

Magnetotactic Bacteria

  • Dennis A. BazylinskiEmail author
  • Christopher T. Lefèvre
  • Dirk Schüler

Abstract

Prokaryotes that exhibit magnetotaxis, collectively known as the magnetotactic bacteria, are those whose direction of motility is influenced by the Earth’s geomagnetic and externally applied magnetic fields. These ubiquitous, aquatic microorganisms represent a morphologically, phylogenetically, and physiologically diverse group that biomineralize unique organelles called magnetosomes that are responsible for the cells’ magnetotactic behavior. Magnetosomes consist of magnetic mineral crystals, either magnetite (Fe3O4) or greigite (Fe3S4), each enveloped by a phospholipid bilayer membrane that contains proteins not present in other membranes. While there are several different magnetite and greigite crystal morphologies, mature crystals of both minerals are always in the single magnetic domain size range, about 35–120 nm, thus having the highest possible magnetic moment per unit volume. In most magnetotactic bacteria, magnetosomes are arranged as a chain within the cell thereby maximizing the magnetic dipole moment of the cell causing the cell to passively align along magnetic field lines as it swims. Magnetotaxis is thought to function in conjunction with chemotaxis in aiding magnetotactic bacteria in locating and maintaining an optimal position in vertical chemical concentration gradients common in stationary aquatic habitats, by reducing a three-dimensional search problem to one of a single dimension.

Although the detection of magnetotactic bacteria in samples collected from natural environments is relatively easy, the magnetotactic bacteria are a fastidious group of prokaryotes and special culture conditions are necessary for their isolation and cultivation. Phylogenetically, most known cultured and uncultured magnetotactic bacteria are associated with the Alpha-, Gamma-, and Deltaproteobacteria classes of the Proteobacteria phylum and the Nitrospirae phylum. All cultured species are either microaerophiles or anaerobes or both. Most cultured species of the Alpha- and Gammaproteobacteria classes are microaerophiles that grow chemolithoautotrophically using reduced sulfur compounds as electron sources and the Calvin-Benson-Bassham cycle or the reverse tricarboxylic acid cycle for autotrophy and chemoorganoheterotrophically using organic acids as electron and carbon sources. Those in the Deltaproteobacteria are sulfate-reducing anaerobes that only grow chemoorganoheterotrophically. Almost all cultured species exhibit nitrogenase activity and thus fix atmospheric nitrogen and many denitrify. Magnetotactic bacteria thus show a great potential for iron, nitrogen, sulfur, and carbon cycling in natural environments.

Genetic determinants for magnetosome synthesis, the mam and mms genes, are organized as clusters in the genomes of all magnetotactic bacteria examined. These clusters are in close proximity to each other within the genomes and are surrounded by genomic features that suggest that magnetosome genes are organized as a magnetosome gene island that might be transmitted to many different bacteria through horizontal gene transfer. Through the development of genetic systems in some magnetotactic bacteria, the functions of several magnetosome membrane proteins in the biomineralization of the magnetite magnetosome chain have been demonstrated although the roles of most remain unknown.

Bacterial magnetosomes have novel physical and magnetic properties and also geological significance and have been used in a large number of commercial and medical applications.

Notes

Acknowledgments

We are grateful to the continued collaboration, support, and encouragement of R. B. Frankel. DAB is supported by US National Science Foundation (NSF) Grant EAR-0920718. CTL is supported by a grant from the Fondation pour la Recherche Médicale SPF20101220993. DS has been supported by grants from the Deutsche Forschungsgemeinschaft, the German Bundesministerium für Bildung und Forschung, and the European Union.

References

  1. Abrajevitch A, Kodama K (2011) Diagenetic sensitivity of paleoenvironmental proxies: a rock magnetic study of Australian continental margin sediments. Geochem Geophys Geosyst 12:Q05Z24CrossRefGoogle Scholar
  2. Abreu F, Silva KT, Martins JL, Lins U (2006) Cell viability in multicellular magnetotactic prokaryotes. Int Microbiol 9:267–271PubMedGoogle Scholar
  3. Abreu F, Martins JL, Silveira TS, Keim CN, Lins de Barros HGP, Filho FJG, Lins U (2007) “Candidatus magnetoglobus multicellularis”, a multicellular, magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol 57:1318–1322PubMedCrossRefGoogle Scholar
  4. Abreu F, Cantão ME, Nicolás MF, Barcellos FG, Morillo V, Almeida LG, Do Nascimento FF, Lefèvre CT, Bazylinski DA, de Vasconcelos ATR, Lins U (2011) Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria. ISME J 5:1634–1640PubMedCrossRefGoogle Scholar
  5. Alphandéry E, Faure S, Raison L, Duguet E, Howse PA, Bazylinski DA (2011) Heat production by bacterial magnetosomes exposed to an oscillating magnetic field. J Phys Chem C 115:18–22CrossRefGoogle Scholar
  6. Alphandery E, Faure S, Seksek O, Guyot F, Chebbi I (2011) Chains of magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy. ACS Nano 5:6279–6296PubMedCrossRefGoogle Scholar
  7. Amann R, Peplies J, Schüler D (2007) Diversity and taxonomy of magnetotactic bacteria. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 25–36CrossRefGoogle Scholar
  8. Amemiya Y, Tanaka T, Yoza B, Matsunaga T (2005) Novel detection system for biomolecules using nano-sized bacterial magnetic particles and magnetic force microscopy. J Biotechnol 120:308–314PubMedCrossRefGoogle Scholar
  9. Arakaki A, Takeyama H, Tanaka T, Matsunaga T (2002) Cadmium recovery by a sulfate-reducing magnetotactic bacterium, Desulfovibrio magneticus RS-1, using magnetic separation. Appl Biochem Biotechnol 98–100:833–840PubMedCrossRefGoogle Scholar
  10. Arakaki A, Webb J, Matsunaga T (2003) A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J Biol Chem 278:8745–8750PubMedCrossRefGoogle Scholar
  11. Arakaki A, Hideshima S, Nakagawa T, Niwa D, Tanaka T, Matsunaga T, Osaka T (2004) Detection of biomolecular interaction between biotin and streptavidin on a self-assembled monolayer using magnetic nanoparticles. Biotechnol Bioeng 88:543–546PubMedCrossRefGoogle Scholar
  12. Arakaki A, Nakazawa H, Nemoto M, Mori T, Matsunaga T (2008) Formation of magnetite by bacteria and its application. J R Soc Interface 5:977–999PubMedCrossRefGoogle Scholar
  13. Arató B, Szányi Z, Flies C, Schüler D, Frankel RB, Buseck PR, Pósfai M (2005) Crystal-size and shape distributions of magnetite from uncultured magnetotactic bacteria as a potential biomarker. Am Mineral 90:1233–1240CrossRefGoogle Scholar
  14. Baeuerlein E (2003) Biomineralization of unicellular organisms: an unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angew Chem Int Ed Engl 42:614–641CrossRefGoogle Scholar
  15. Bahaj AS, James PAB, Ellwood DC, Watson JHP (1993) Characterization and growth of magnetotactic bacteria-implications of clean up of environmental pollution. J Appl Physiol 73:5394–5396CrossRefGoogle Scholar
  16. Bahaj AS, James PAB, Moeschler FD (1998a) Low magnetic-field separation system for metal-loaded magnetotactic bacteria. J Magn Magn Mater 177:1453–1454CrossRefGoogle Scholar
  17. Bahaj AS, Croudace IW, James PAB, Moeschler FD, Warwick PE (1998b) Continuous radionuclide recovery from wastewater using magnetotactic bacteria. J Magn Magn Mater 184:241–244CrossRefGoogle Scholar
  18. Bahaj AS, James PAB, Moeschler FD (1998c) Wastewater treatment by biomagnetic separation: a comparison of iron oxide and iron sulphide biomass recovery. Water Sci Technol 38:311–317Google Scholar
  19. Balkwill DL, Maratea D, Blakemore RP (1980) Ultrastructure of a magnetic spirillum. J Bacteriol 141:1399–1408PubMedGoogle Scholar
  20. Bazylinski DA (1995) Structure and function of the bacterial magnetosome. ASM News 61:337–343Google Scholar
  21. Bazylinski DA, Blakemore RP (1983a) Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Appl Environ Microbiol 46:1118–1124PubMedGoogle Scholar
  22. Bazylinski DA, Blakemore RP (1983b) Nitrogen fixation (acetylene reduction) in Aquaspirillum magnetotacticum. Curr Microbiol 9:305–308CrossRefGoogle Scholar
  23. Bazylinski DA, Frankel RB (1992) Production of iron sulfide minerals by magnetotactic bacteria from sulfidic environments. In: Skinner HCW, Fitzpatrick RW (eds) Biomineralization processes of iron and manganese: modern and ancient environments. Catena-Verlag, Cremlingen-Destedt, pp 147–159Google Scholar
  24. Bazylinski DA, Frankel RB (2000) Magnetic iron oxide and iron sulfide minerals within microorganisms. In: Bäuerlein E (ed) Biomineralization: from biology to biotechnology and medical application. Wiley-VCH, Weinheim, pp 25–46Google Scholar
  25. Bazylinski DA, Frankel RB (2003) Biologically controlled mineralization in prokaryotes. Rev Mineral Geochem 54:95–114CrossRefGoogle Scholar
  26. Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217–230PubMedCrossRefGoogle Scholar
  27. Bazylinski DA, Moskowitz BM (1997) Microbial biomineralization of magnetic iron minerals: microbiology, magnetism and environmental significance. Rev Mineral 35:181–223Google Scholar
  28. Bazylinski DA, Schübbe S (2007) Controlled biomineralization by and applications of magnetotactic bacteria. Adv Appl Microbiol 62:21–62PubMedCrossRefGoogle Scholar
  29. Bazylinski DA, Williams TJ (2007) Ecophysiology of magnetotactic bacteria. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 37–75CrossRefGoogle Scholar
  30. Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic production of magnetite by a marine magnetotactic bacterium. Nature 334:518–519CrossRefGoogle Scholar
  31. Bazylinski DA, Frankel RB, Garratt-Reed AJ, Mann S (1990) Biomineralization of iron-sulfides in magnetotactic bacteria from sulfidic environments. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum, New York, pp 239–255Google Scholar
  32. Bazylinski DA, Garratt-Reed AJ, Abedi A, Frankel RB (1993a) Copper association with iron sulfide magnetosomes in a magnetotactic bacterium. Arch Microbiol 160:35–42Google Scholar
  33. Bazylinski DA, Heywood BR, Mann S, Frankel RB (1993b) Fe3O4 and Fe3S4 in a bacterium. Nature 366:218–219CrossRefGoogle Scholar
  34. Bazylinski DA, Garratt-Reed A, Frankel RB (1994) Electron-microscopic studies of magnetosomes in magnetotactic bacteria. Microscopy Res Tech 27:389–401CrossRefGoogle Scholar
  35. Bazylinski DA, Frankel RB, Heywood BR, Mann S, King JW, Donaghay PL, Hanson AK (1995) Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl Environ Microbiol 61:3232–3239PubMedGoogle Scholar
  36. Bazylinski DA, Dean AJ, Schüler D, Phillips EJP, Lovley DR (2000) N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ Microbiol 2:266–273PubMedCrossRefGoogle Scholar
  37. Bazylinski DA, Dean AJ, Williams TJ, Kimble Long L, Middleton SL, Dubbels BL (2004) Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 182:373–387PubMedCrossRefGoogle Scholar
  38. Bazylinski DA, Williams TJ, Lefèvre CT, Berg RJ, Zhang CL, Bowser SS, Dean AJ, Beveridge TJ (2012a) Magnetococcus marinus gen. nov., sp. nov., a marine, magnetotactic bacterium that represents a novel lineage (Magnetococcaceae fam. nov.; Magnetococcales ord. nov.) at the base of the Alphaproteobacteria. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.038927-0Google Scholar
  39. Bazylinski DA, Williams TJ, Lefèvre CT, Trubitsyn D, Fang J, Beveridge TJ, Moskowitz BM, Ward B, Schübbe S, Dubbels BL, Simpson B (2012b) Magnetovibrio blakemorei, gen. nov. sp. nov., a new magnetotactic bacterium (Alphaproteobacteria: Rhodospirillaceae) isolated from a salt marsh. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.044453-0Google Scholar
  40. Bellini S (1963) On a unique behavior of freshwater bacteria. University of Pavia, Institute of Microbiology, PaviaGoogle Scholar
  41. Bellini S (2009a) On a unique behavior of freshwater bacteria. Chin J Oceanol Limnol 27:3–5CrossRefGoogle Scholar
  42. Bellini S (2009b) Further studies on “magnetosensitive bacteria”. Chin J Oceanol Limnol 27:6–12CrossRefGoogle Scholar
  43. Berner RA (1967) Thermodynamic stability of sedimentary iron sulfides. Am J Sci 265:773–785CrossRefGoogle Scholar
  44. Berner RA (1970) Sedimentary pyrite formation. Am J Sci 268:1–23CrossRefGoogle Scholar
  45. Berner RA (1974) Iron sulfides in Pleistocene deep Black Sea sediments and their palaeooceanographic significance. In: Degens ET, and Ross DA (eds) The Black Sea: geology, chemistry and biology. AAPG Memoirs 20:American Association of Petroleum Geologists. Tulsa, OK, pp 524–531Google Scholar
  46. Bertani LE, Weko J, Phillips KV, Gray RF, Kirschvink JL (2001) Physical and genetic characterization of the genome of Magnetospirillum magnetotacticum, strain MS-1. Gene 264:257–263PubMedCrossRefGoogle Scholar
  47. Blakemore RP (1975) Magnetotactic bacteria. Science 190:377–379PubMedCrossRefGoogle Scholar
  48. Blakemore RP (1982) Magnetotactic bacteria. Annu Rev Microbiol 36:217–238PubMedCrossRefGoogle Scholar
  49. Blakemore RP, Maratea D, Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140:720–729PubMedGoogle Scholar
  50. Blakemore RP, Frankel RB, Kalmijn AJ (1980) South-seeking magnetotactic bacteria in the southern-hemisphere. Nature 286:384–385CrossRefGoogle Scholar
  51. Blakemore RP, Short KA, Bazylinski DA, Rosenblatt C, Frankel RB (1985) Microaerobic conditions are required for magnetite synthesis within Aquaspirillum magnetotacticum. Geomicrobiol J 4:53–71CrossRefGoogle Scholar
  52. Blum G, Ott M, Lischewski A, Ritter A, Imrich H, Tschäpe H, Hacker J (1994) Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun 62:606–614PubMedGoogle Scholar
  53. Borchardt-Ott W (2011) Crystallography: an introduction, 3rd edn. Springer, Berlin/Heidelberg, 373Google Scholar
  54. Braatsch S, Moskvin OV, Klug G, Gomelsky M (2004) Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J Bacteriol 186:7726–7735PubMedCrossRefGoogle Scholar
  55. Burgess JG, Kawaguchi R, Sakaguchi T, Thornhill RH, Matsunaga T (1993) Evolutionary relationships among Magnetospirillum strains inferred from phylogenetic analysis of 16S rDNA sequences. J Bacteriol 175:6689–6694PubMedGoogle Scholar
  56. Buseck PR, Dunin-Borkowski RE, Devouard B, Frankel RB, McCartney MR, Midgley PA, Pósfai M, Weyland M (2001) Magnetite morphology and life on mars. Proc Natl Acad Sci USA 98:13490–13495PubMedCrossRefGoogle Scholar
  57. Butler RF, Banerjee SK (1975) Theoretical single-domain grain size range in magnetite and titanomagnetite. J Geophys Res 80:4049–4058CrossRefGoogle Scholar
  58. Byrne ME, Ball DA, Guerquin-Kern JL, Rouiller I, Wu TD, Downing KH, Vali H, Komeili A (2010) Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes. Proc Natl Acad Sci USA 107:12263–12268PubMedCrossRefGoogle Scholar
  59. Cabeen MT, Jacobs-Wagner C (2010) The bacterial cytoskeletan. Annu Rev Genet 44:365–392PubMedCrossRefGoogle Scholar
  60. Calugay RJ, Miyashita H, Okamura Y, Matsunaga T (2003) Siderophore production by the magnetic bacterium Magnetospirillum magneticum AMB-1. FEMS Microbiol Lett 218:371–375PubMedCrossRefGoogle Scholar
  61. Carballido-Lopez R (2006) The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70:888–909PubMedCrossRefGoogle Scholar
  62. Chang S-BR, Kirschvink JL (1989) Magnetofossils, the magnetization of sediments, and the evolution of magnetite biomineralization. Annu Rev Earth Planet Sci 17:169–195CrossRefGoogle Scholar
  63. Chang S-BR, Stolz JF, Kirschvink JL, Awramik SM (1989) Biogenic magnetite in stromatolites. 2: occurrence in ancient sedimentary environments. Precambrian Res 43:305–312CrossRefGoogle Scholar
  64. Chertok B, David AE, Huang Y, Yang VC (2007) Glioma selectivity of magnetically targeted nanoparticles: a role of abnormal tumor hydrodynamics. J Control Release 122:315–323PubMedCrossRefGoogle Scholar
  65. Ciofani G, Riggio C, Raffa V, Menciassi A, Cuschieri A (2009) A bi-modal approach against cancer: magnetic alginate nanoparticles for combined chemotherapy and hyperthermia. Med Hypotheses 73:80–82PubMedCrossRefGoogle Scholar
  66. Clemett SJ, Thomas-Keprta KL, Shimmin J, Morphew M, McIntosh JR, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson EK Jr, Romanek CS (2002) Crystal morphology of MV-1 magnetite. Am Mineral 87:1727–1730Google Scholar
  67. Cox BL, Popa R, Bazylinski DA, Lanoil D, Douglas S, Belz A, Engler DL, Nealson KH (2002) Organization and elemental analysis of P-, S-, and Fe-rich inclusions in a population of freshwater magnetococci. Geomicrobiol J 19:387–406CrossRefGoogle Scholar
  68. de Graef MR, Alexeeva S, Snoep JL, De Mattos MJT (1999) The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. J Bacteriol 181:2351–2357PubMedGoogle Scholar
  69. Dean AJ, Bazylinski DA (1999) Genome analysis of several marine, magnetotactic bacterial strains by pulsed-field gel electrophoresis. Curr Microbiol 39:219–225PubMedCrossRefGoogle Scholar
  70. DeLong EF, Frankel RB, Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259:803–806PubMedCrossRefGoogle Scholar
  71. Demitrack A (1985) A search for bacterial magnetite in the sediments of Eel Pond, Woods Hole, Massachusetts. In: Kirschvink JL, Jones DS, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms. Plenum, New York, pp 625–645CrossRefGoogle Scholar
  72. Derman AI, Becker EC, Truong BD, Fujioka A, Tucey TM, Erb ML, Patterson PC, Pogliano J (2009) Phylogenetic analysis identifies many uncharacterized actin-like proteins (Alps) in bacteria: regulated polymerization, dynamic instability and treadmilling in Alp7A. Mol Microbiol 73:534–552PubMedCrossRefGoogle Scholar
  73. Devouard B, Pósfai M, Hua X, Bazylinski DA, Frankel RB, Buseck PR (1998) Magnetite from magnetotactic bacteria: size distribution and twining. Am Mineral 83:1387–1398Google Scholar
  74. Diaz-Ricci JC, Kirschvink JL (1992) Magnetic domain state and coercivity predictions for biogenic greigite (Fe3S4): a comparison of theory with magnetosome observations. J Geophys Res 97(B12):17309–17315CrossRefGoogle Scholar
  75. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424PubMedCrossRefGoogle Scholar
  76. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Söldner R, Carballido-López R (2011) Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225–228PubMedCrossRefGoogle Scholar
  77. Draper O, Byrne ME, Li Z, Keyhani S, Barrozo JC, Jensen G, Komeili A (2011) MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Mol Microbiol 82:342–354PubMedCrossRefGoogle Scholar
  78. Dubbels BL, DiSpirito AA, Morton JD, Semrau JD, Neto JN, Bazylinski DA (2004) Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1. Microbiology 150:2931–2945PubMedCrossRefGoogle Scholar
  79. Duguet E, Mornet S, Vasseur S, Devoisselle JM (2006) Magnetic nanoparticles and their applications in medicine. Nanomedicine 1:157–168PubMedCrossRefGoogle Scholar
  80. Dunin-Borkowski RE, McCartney MR, Frankel RB, Bazylinski DA, Pósfai M, Buseck PR (1998) Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282:1868–1870PubMedCrossRefGoogle Scholar
  81. Dunin-Borkowski RE, McCartney MR, Pósfai M, Frankel RB, Bazylinski DA, Buseck PR (2001) Off-axis electron holography of magnetotactic bacteria: magnetic microstructure of strains MV-1 and MS-1. Eur J Mineral 13:671–684CrossRefGoogle Scholar
  82. Dutz S, Hergt R, Mürbe J, Töpfer J, Müller R, Zeisberger M, Andrä W, Bellemann ME (2005) Magnetic nanoparticles for biomedical heating applications. Z Phys Chem 220:145–151CrossRefGoogle Scholar
  83. Dutz S, Hergt R, Mürbe J, Müller R, Zeisberger M, Andrä W, Töpfer J, Bellemann ME (2007) Hysteresis losses of magnetic nanoparticle powders in the single domain size range. J Magn Magn Mater 308:305–312CrossRefGoogle Scholar
  84. Evans ME, Heller F (2003) Environmental magnetism: principles and applications of enviromagnetics. Academic, San Diego, 311Google Scholar
  85. Faivre D, Bottger LH, Matzanke BF, Schüler D (2007) Intracellular magnetite biomineralization in bacteria proceeds by a distinct pathway involving membrane-bound ferritin and an iron(II) species. Angew Chem Int Ed 46:8495–8499CrossRefGoogle Scholar
  86. Faivre D, Menguy N, Pósfai M, Schüler D (2008) Environmental parameters affect the physical properties of fast-growing magnetosomes. Am Mineral 93:463–469CrossRefGoogle Scholar
  87. Faivre D, Fischer A, Garcia-Rubio I, Mastrogiacomo G, Gehring AU (2010) Development of cellular magnetic dipoles in magnetotactic bacteria. Biophys J 99:1268–1273PubMedCrossRefGoogle Scholar
  88. Fanning AS, Anderson JM (1996) Protein-protein interactions: PDZ domain networks. Curr Biol 6:1385–1388PubMedCrossRefGoogle Scholar
  89. Farina M, Lins de Barros H, Esquivel DMS, Danon J (1983) Ultrastructure of a magnetotactic bacterium. Biol Cell 48:85–88Google Scholar
  90. Farina M, Motta de Esquivel D, Lins de Barros HGP (1990) Magnetic iron-sulphur crystals from a magnetotactic microorganism. Nature 343:256–258CrossRefGoogle Scholar
  91. Farina M, Kachar B, Lins U, Broderick R, Lins de Barros HGP (1994) The observation of large magnetite (Fe3O4) crystals from magnetotactic bacteria by electron and atomic force microscopy. J Microsc 173:1–8CrossRefGoogle Scholar
  92. Fassbinder JWE, Stanjek H, Vali H (1990) Occurrence of magnetic bacteria in soil. Nature 343:161–162PubMedCrossRefGoogle Scholar
  93. Figge RM, Divakaruni AV, Gober JW (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51:1321–1332PubMedCrossRefGoogle Scholar
  94. Flies CB, Jonkers HM, de Beer D, Bosselmann K, Böttcher ME, Schüler D (2005a) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 52:185–195PubMedCrossRefGoogle Scholar
  95. Flies CB, Peplies J, Schüler D (2005b) Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol 71:2723–2731PubMedCrossRefGoogle Scholar
  96. Frankel RB (1984) Magnetic guidance of organisms. Annu Rev Biophys Biomol Struct 13:85–103CrossRefGoogle Scholar
  97. Frankel RB, Bazylinski DA (2004) Magnetosome mysteries. ASM News 70:176–183Google Scholar
  98. Frankel RB, Blakemore RP (1980) Navigational compass in freshwater magnetotactic bacteria. J Magn Magn Mater 15–18:1562–1564CrossRefGoogle Scholar
  99. Frankel RB, Moskowitz BM (2003) Biogenic magnets. In: Miller JS, Drillon M (eds) Magnetism: molecules to materials IV. Wiley-VCH, Weinheim, pp 205–231Google Scholar
  100. Frankel RB, Blakemore RP, Wolfe RS (1979) Magnetite in freshwater magnetic bacteria. Science 203:1355–1357PubMedCrossRefGoogle Scholar
  101. Frankel RB, Papaefthymiou GC, Blakemore RP, O’Brien W (1983) Fe3O4 precipitation in magnetotactic bacteria. Biochim Biophys Acta 763:147–159CrossRefGoogle Scholar
  102. Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J73:994–1000CrossRefGoogle Scholar
  103. Frankel RB, Bazylinski DA, Schüler D (1998) Biomineralization of magnetic iron minerals in magnetotactic bacteria. Supramol Sci 5:383–390CrossRefGoogle Scholar
  104. Frankel RB, Williams TJ, Bazylinski DA (2007) Magneto-aerotaxis. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Heidelberg, pp 1–24CrossRefGoogle Scholar
  105. Fukuda Y, Okamura Y, Takeyama H, Matsunaga T (2006) Dynamic analysis of a genomic island in Magnetospirillum sp. strain AMB-1 reveals how magnetosome synthesis developed. FEBS Lett 580:801–812PubMedCrossRefGoogle Scholar
  106. Funaki M, Sakai H, Matsunaga T (1989) Identification of the magnetic poles on strong magnetic grains from meteorites using magnetotactic bacteria. J Geomagn Geoelectr 41:77–87CrossRefGoogle Scholar
  107. Funaki M, Sakai H, Matsunaga T, Hirose S (1992) The S-pole distribution on magnetic grains in pyroxenite determined by magnetotactic bacteria. Phys Earth Planet Inter 70:253–260CrossRefGoogle Scholar
  108. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T (2011) Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:222–225PubMedCrossRefGoogle Scholar
  109. Geelhoed JS, Kleerebezem R, Sorokin DY, Stams AJM, van Loosdrecht MCM (2010) Reduced inorganic sulfur oxidation supports autotrophic and mixotrophic growth of Magnetspirillum strain J10 and Magnetospirillum gryphiswaldense. Environ Microbiol 12:1031–1040PubMedCrossRefGoogle Scholar
  110. Gehring A, Kind J, Charilaou M, García-Rubio I (2011) The detection of magnetotactic bacteria and magnetofossils by means of magnetic anisotropy. Earth Planet Sci Lett 309:113–117CrossRefGoogle Scholar
  111. Ginet N, Pardoux R, Adryanczyk G, Garcia D, Brutesco C, Pignol D (2011) Single-step production of a recyclable nanobiocatalyst for scavenging organophosphate pesticides using functionalized bacterial magnetosomes. PLoS One 6:e21442PubMedCrossRefGoogle Scholar
  112. Glöckl G, Hergt R, Zeisberger M, Dutz S, Nagel S, Weitschies W (2006) Effect of field parameters, nanoparticle properties and immobilization on the specific heating power in magnetic particle hyperthermia. JPhys Condens Matter 18:S2935–S2949CrossRefGoogle Scholar
  113. Gorby YA, Beveridge TJ, Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170:834–841PubMedGoogle Scholar
  114. Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183:9–18PubMedCrossRefGoogle Scholar
  115. Greenberg M, Canter K, Mahler I, Tornheim A (2005) Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. Biophys J 88:1496–1499PubMedCrossRefGoogle Scholar
  116. Grünberg K, Wawer C, Tebo BM, Schüler D (2001) A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Appl Environ Microbiol 67:4573–4582PubMedCrossRefGoogle Scholar
  117. Grünberg K, Müller EC, Otto A, Reszka R, Linder D, Kube M, Reinhardt R, Schüler D (2004) Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 70:1040–1050PubMedCrossRefGoogle Scholar
  118. Haney CJ, Grass G, Franke S, Rensing C (2005) New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol 32:215–226PubMedCrossRefGoogle Scholar
  119. Hanson TE, Tabita FR (2001) A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA 98:4397–4402PubMedCrossRefGoogle Scholar
  120. Hanzlik M, Winklhofer M, Petersen N (1996) Spatial arrangement of chains of magnetosomes in magnetotactic bacteria. Earth Planet Sci Lett 145:125–134CrossRefGoogle Scholar
  121. Hanzlik M, Winklhofer M, Petersen N (2002) Pulsed-field-remanence measurements on individual magnetotactic bacteria. J Magn Magn Mater 248:258–267CrossRefGoogle Scholar
  122. Harasko G, Pfützner H, Rapp E, Futschik K, Schüler D (1993) Determination of the concentration of magnetotactic bacteria by means of susceptibility measurements. Jpn J Appl Phys 32(Part 1):252–260CrossRefGoogle Scholar
  123. Harasko G, Pfützner H, Futschik K (1995) Domain analysis by means of magnetotactic bacteria. IEEE Trans Magn 31:938–949CrossRefGoogle Scholar
  124. Hergt R, Andrä W, D’Ambly CG, Higler I, Kaiser WA, Richter U, Schmidt HG (1998) Physical limits of hyperthermia using magnetite fine particles. IEEE Trans Magn 34:3745–3754CrossRefGoogle Scholar
  125. Hergt R, Hiergeist R, Hilger I, Kaiser WA (2002) Magnetic nanoparticles for thermoablation. Recent Res Dev Mater Sci 3:723–742Google Scholar
  126. Hergt R, Hiergeist R, Zeisberger M, Schüler D, Heyen U, Hilger I, Kaiser WA (2005) Magnetic properties of bacterial magnetosomes as potential diagnostic and therapeutic tools. J Magn Magn Mater 293:80–86CrossRefGoogle Scholar
  127. Hergt R, Dutz S, Müller R, Zeisberger M (2006) Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy. J Phys Condens Matter 18:S2919–S2934CrossRefGoogle Scholar
  128. Heyen U, Schüler D (2003) Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermenter. Appl Microbiol Biotechnol 61:536–544PubMedGoogle Scholar
  129. Heywood BR, Bazylinski DA, Garratt-Reed AJ, Mann S, Frankel RB (1990) Controlled biosynthesis of greigite (Fe3S4) in magnetotactic bacteria. Naturwissenschaften 77:536–538CrossRefGoogle Scholar
  130. Heywood BR, Mann S, Frankel RB (1991) Structure, morphology and growth of biogenic greigite (Fe3S4). In: Alpert M, Calvert P, Frankel RB, Rieke P, Tirrell D (eds) Materials synthesis based on biological processes. Materials Research Society, Pittsburgh, pp 93–108Google Scholar
  131. Hilger I, Andrä W, Hergt R, Hiergeist R, Schubert H, Kaiser WA (2001) Electromagnetic heating of breast tumors in interventional radiology: in vitro and in vivo studies in human cadavers and mice. Radiology 218:570–575PubMedGoogle Scholar
  132. Hilger I, Hergt R, Kaiser WA (2005) Use of magnetic nanoparticle heating in the treatment of breast cancer. IEE Proc Nanobiotechnol 152:33–39PubMedCrossRefGoogle Scholar
  133. Hoffman PS, Pine L, Bell S (1983) Production of superoxide and hydrogen peroxide in medium used to culture Legionella pneumophila: catalytic decomposition by charcoal. Appl Environ Microbiol 45:784–791PubMedGoogle Scholar
  134. Huettel M, Forster S, Kloser S, Fossing H (1996) Vertical migration in the sediment-dwelling sulfur bacteria Thioploca spp. in overcoming diffusion limitations. Appl Environ Microbiol 62:1863–1872PubMedGoogle Scholar
  135. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376PubMedGoogle Scholar
  136. Isambert A, Menguy N, Larquet E, Guyot F, Valet J-P (2007) Transmission electron microscopy study of magnetites in a freshwater population of magnetotactic bacteria. Am Mineral 92:621–630CrossRefGoogle Scholar
  137. Ito A, Honda H, Kobayashi T (2006) Cancer immunotherapy based on intracellular hyperthermia using magnetite nanoparticles: a novel concept of “heat-controlled necrosis” with heat shock protein expression. Cancer Immunol Immunother 55:320–328PubMedCrossRefGoogle Scholar
  138. Jimenez-Lopez C, Romanek CS, Bazylinski DA (2010) Magnetite as a prokaryotic biomarker: a review. J Geophys Res-Biogeo 115:G00G03CrossRefGoogle Scholar
  139. Jogler C, Schüler D (2007) Genetic analysis of magnetosome biomineralization. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 133–161CrossRefGoogle Scholar
  140. Jogler C, Kube M, Schübbe S, Ullrich S, Teeling H, Bazylinski DA, Reinhardt R, Schüler D (2009a) Comparative analysis of magnetosome gene clusters in magnetotactic bacteria provides further evidence for horizontal gene transfer. Environ Microbiol 11:1267–1277PubMedCrossRefGoogle Scholar
  141. Jogler C, Lin W, Meyerdierks A, Kube M, Katzmann E, Flies C, Pan Y, Amann R, Reinhardt R, Schüler D (2009b) Toward cloning of the magnetotactic metagenome: identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol 75:3972–3979PubMedCrossRefGoogle Scholar
  142. Jogler C, Niebler M, Lin W, Kube M, Wanner G, Kolinko S, Stief P, Beck AJ, de Beer D, Petersen N, Pan Y, Amann R, Reinhardt R, Schüler D (2010) Cultivation-independent characterization of ‘Candidatus Magnetobacterium bavaricum’ via ultrastructural, geochemical, ecological and metagenomic methods. Environ Microbiol 12:2466–2478PubMedCrossRefGoogle Scholar
  143. Jogler C, Wanner G, Kolinko S, Niebler M, Amann R, Petersen N, Kube M, Reinhardt R, Schüler D (2011) Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proc Natl Acad Sci USA 108:1134–1139PubMedCrossRefGoogle Scholar
  144. Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922PubMedCrossRefGoogle Scholar
  145. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393PubMedCrossRefGoogle Scholar
  146. Katzmann E, Scheffel A, Gruska M, Plitzko JM, Schüler D (2010) Loss of the actin-like protein MamK has pleiotropic effects on magnetosome formation and chain assembly in Magnetospirillum gryphiswaldense. Mol Microbiol 77:208–224PubMedCrossRefGoogle Scholar
  147. Katzmann E, Müller FD, Lang C, Messerer M, Winklhofer M, Plitzko JM, Schüler D (2011) Magnetosome chains are recruited to cellular division sites and split by asymmetric septation. Mol Microbiol 82:1316–1329PubMedCrossRefGoogle Scholar
  148. Keim CN, Lins U, Farina M (2003) Iron oxide and iron sulfide crystals in magnetotactic multicellular aggregates. Acta Microsc 12:3–4Google Scholar
  149. Keim CN, Abreu F, Lins U, Lins de Barros HGP, Farina M (2004a) Cell organization and ultrastructure of a magnetotactic multicellular organism. J Struct Biol 145:254–262PubMedCrossRefGoogle Scholar
  150. Keim CN, Martins JL, Abreu F, Rosado AS, Lins de Barros HGP, Borojevic R, Lins U, Farina M (2004b) Multicellular life cycle of magnetotactic multicellular prokaryotes. FEMS Microbiol Lett 240:203–208PubMedCrossRefGoogle Scholar
  151. Keim CN, Martins JL, Lins de Barros HGP, Lins U, Farina M (2007) Structure, behavior, ecology and diversity of multicellular magnetotactic prokaryotes. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 103–132CrossRefGoogle Scholar
  152. Keim CN, Lins U, Farina M (2009) Manganese in biogenic magnetite crystals from magnetotactic bacteria. FEMS Microbiol Lett 292:250–253PubMedCrossRefGoogle Scholar
  153. Kim BY, Kodama KP, Moeller RE (2005) Bacterial magnetite produced in water column dominates lake sediment mineral magnetism: Lake Ely, USA. Geophys J Int 163:26–37CrossRefGoogle Scholar
  154. Kind J, Gehring AU, Winklhofer M, Hirt AM (2011) Combined use of magnetometry and spectroscopy for identifying magnetofossils in sediments. Geochem Geophy Geosy 12:Q08008CrossRefGoogle Scholar
  155. Kolinko I, Jogler C, Katzmann E, Schüler D (2011) Frequent mutations within the genomic magnetosome island of Magnetospirillum gryphiswaldense are mediated by RecA. J Bacteriol 193:5328–5334PubMedCrossRefGoogle Scholar
  156. Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler D (2012) Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environ Microbiol 14:1709–1721PubMedCrossRefGoogle Scholar
  157. Komeili A (2007a) Cell biology of magnetosome formation. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 163–174CrossRefGoogle Scholar
  158. Komeili A (2007b) Molecular mechanisms of magnetosome formation. Annu Rev Biochem 76:351–356PubMedCrossRefGoogle Scholar
  159. Komeili A, Vali H, Beveridge TJ, Newman DK (2004) Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc Natl Acad Sci USA 101:3839–3844PubMedCrossRefGoogle Scholar
  160. Komeili A, Li Z, Newman DK, Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242–245PubMedCrossRefGoogle Scholar
  161. Kopp RE, Kirschvink JL (2008) The identification and biogeochemical interpretation of fossil magnetotactic bacteria. Earth Sci Rev 86:42–61CrossRefGoogle Scholar
  162. Krieg NR, Hoffman PS (1986) Microaerophily and oxygen toxicity. Annu Rev Microbiol 40:107–130PubMedCrossRefGoogle Scholar
  163. Kuhara M, Takeyama H, Tanaka T, Matsunaga T (2004) Magnetic cell separation using antibody binding with protein A expressed on bacterial magnetic particles. Anal Chem 76:6207–6213PubMedCrossRefGoogle Scholar
  164. Lang C, Schüler D (2006) Biogenic nanoparticles: production, characterization, and application of bacterial magnetosomes. J Phys Condens Matter 18:S2815–S2828CrossRefGoogle Scholar
  165. Lang C, Schüler D, Faivre D (2007) Synthesis of magnetite nanoparticles for bio- and nanotechnology: genetic engineering and biomimetics of bacterial magnetosomes. Macromol Biosci 7:144–151PubMedCrossRefGoogle Scholar
  166. Lee J-H, Huh Y-M, Jun Y-W, Seo J-W, Jang J-T, Song H-T, Kim S, Cho E-J, Yoon H-G, Suh J-S, Cheon J (2007) Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nat Med 13:95–99PubMedCrossRefGoogle Scholar
  167. Lefèvre C, Bernadac A, Pradel N, Wu LF, Yu-Zhang K, Xiao T, Yonnet JP, Lebouc A, Song T, Fukumori Y (2007) Characterization of Mediterranean magnetotactic bacteria. J Ocean Univ China (Oceanic and Coastal Sea Research) 6:355–359CrossRefGoogle Scholar
  168. Lefèvre CT, Bernadac A, Yu-Zhang K, Pradel N, Wu LF (2009) Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ Microbiol 11:1646–1657PubMedCrossRefGoogle Scholar
  169. Lefèvre CT, Abreu F, Lins U, Bazylinski DA (2010a) Non-magnetotactic multicellular prokaryotes from low saline, nonmarine aquatic environments and their unusual negative phototactic behavior. Appl Environ Microbiol 76:3220–3227PubMedCrossRefGoogle Scholar
  170. Lefèvre CT, Abreu F, Schmidt ML, Lins U, Frankel RB, Hedlund BP, Bazylinski DA (2010b) Moderately thermophilic magnetotactic bacteria from hot springs in Nevada USA. Appl Environ Microbiol 76:3740–3743PubMedCrossRefGoogle Scholar
  171. Lefèvre CT, Santini CL, Bernadac A, Zhang WJ, Li Y, Wu LF (2010c) Calcium ion-mediated assembly and function of glycosylated flagellar sheath of marine magnetotactic bacterium. Mol Microbiol 78:1304–1312PubMedCrossRefGoogle Scholar
  172. Lefèvre CT, Frankel RB, Abreu F, Lins U, Bazylinski DA (2011a) Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ Microbiol 13:538–549PubMedCrossRefGoogle Scholar
  173. Lefèvre CT, Frankel RB, Pósfai M, Prozorov T, Bazylinski DA (2011b) Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ Microbiol 13:2342–2350PubMedCrossRefGoogle Scholar
  174. Lefèvre CT, Pósfai M, Abreu F, Lins U, Frankel RB, Bazylinski DA (2011c) Morphological features of elongated-anisotropic magnetosome crystals in magnetotactic bacteria of the Nitrospirae phylum and the Deltaproteobacteria class. Earth Planet Sci Lett 312:194–200CrossRefGoogle Scholar
  175. Lefèvre CT, Menguy N, Abreu F, Lins U, Pósfai M, Prozorov T, Pignol D, Frankel RB, Bazylinski DA (2011d) A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 334:1720–1723PubMedCrossRefGoogle Scholar
  176. Lefèvre CT, Viloria N, Schmidt ML, Pósfai M, Frankel RB, Bazylinski DA (2012) Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J 6:440–450PubMedCrossRefGoogle Scholar
  177. Li J, Pan Y, Liu Q, Yu-Zhang K, Menguy N, Che R, Qin H, Lin W, Wu W, Petersen N, Yang X (2010) Biomineralization, crystallography and magnetic properties of bullet-shaped magnetite magnetosomes in giant rod magnetotactic bacteria. Earth Planet Sci Lett 293:368–376CrossRefGoogle Scholar
  178. Lin W, Pan Y (2009) Uncultivated magnetotactic cocci from Yuandadu Park in Beijing. China Appl Environ Microbiol 75:4046–4052CrossRefGoogle Scholar
  179. Lin W, Tian L, Li J, Pan Y (2008) Does capillary racetrack-based enrichment reflect the diversity of uncultivated magnetotactic cocci in environmental samples? FEMS Microbiol Lett 279:202–206PubMedCrossRefGoogle Scholar
  180. Lin W, Li J, Schüler D, Jogler C, Pan Y (2009) Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. Syst Appl Microbiol 5:342–350CrossRefGoogle Scholar
  181. Lin W, Li J, Pan Y (2012) Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl Environ Microbiol 78:668–675PubMedCrossRefGoogle Scholar
  182. Lins U, Farina M (1999) Organisation of cells in magnetotactic multicellular aggregates. Microbiol Res 154:9–13CrossRefGoogle Scholar
  183. Lins U, Freitas F, Keim CN, Farina M (2000) Electron spectroscopic imaging of magnetotactic bacteria: magnetosome morphology and diversity. Microsc Microanal 6:463–470PubMedGoogle Scholar
  184. Lins U, McCartney MR, Farina M, Buseck PR, Frankel RB (2005) Crystal habits and magnetic microstructures of magnetosomes in coccoid magnetotactic bacteria. Appl Environ Microbiol 71:4902–4905PubMedCrossRefGoogle Scholar
  185. Lins U, Keim CN, Evans FF, Buseck PR, Farina M (2007) Magnetite (Fe3O4) and greigite (Fe3S4) crystals in multicellular magnetotactic prokaryotes. Geomicrobiol J 24:43–50CrossRefGoogle Scholar
  186. Lipinska B, Fayet O, Baird L, Georgopoulos C (1989) Identification, characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J Bacteriol 171:1574–1584PubMedGoogle Scholar
  187. Liu Y, Li GR, Guo FF, Jiang W, Li Y, Li LJ (2010) Large-scale production of magnetosomes by chemostat culture of Magnetospirillum gryphiswaldense at high cell density. Microb Cell Fact 9:99PubMedCrossRefGoogle Scholar
  188. Lohße A, Ullrich S, Katzmann E, Borg S, Wanner G, Richter M, Voigt B, Schweder T, Schüler D (2011) Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense: the mamAB operon is sufficient for magnetite biomineralization. PLoS One 6:e25561PubMedCrossRefGoogle Scholar
  189. Mahillon J, Chandler M (1998) Insertion sequences. Microbiol Mol Biol Rev 62:725–774PubMedGoogle Scholar
  190. Mahillon J, Leonard C, Chandler M (1999) IS elements as constituents of bacterial genomes. Res Microbiol 150:675–687PubMedCrossRefGoogle Scholar
  191. Mann S, Frankel RB (1989) Magnetite biomineralization in unicellular organisms. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: chemical and biochemical perspectives. VCH, New York, pp 389–426Google Scholar
  192. Mann S, Frankel RB, Blakemore RP (1984a) Structure, morphology and crystal growth of bacterial magnetite. Nature 405:405–407CrossRefGoogle Scholar
  193. Mann S, Moench TT, Williams RJP (1984b) A high resolution electron microscopic investigation of bacterial magnetite. Proc Roy Soc Lond B Bio 221:385–393CrossRefGoogle Scholar
  194. Mann S, Sparks NHC, Blakemore RP (1987a) Ultrastructure and characterization of anisotropic inclusions in magnetotactic bacteria. Proc Roy Soc Lond B Bio 231:469–476CrossRefGoogle Scholar
  195. Mann S, Sparks NHC, Blakemore RP (1987b) Structure, morphology and crystal growth of anisotropic magnetite crystals in magnetotactic bacteria. Proc Roy Soc Lond B Bio 231:477–487CrossRefGoogle Scholar
  196. Mann S, Sparks NCH, Board RG (1990a) Magnetotactic bacteria: microbiology, biomineralization, palaeomagnetism, and biotechnology. Adv Microbial Phys 31:125–181CrossRefGoogle Scholar
  197. Mann S, Sparks NHC, Frankel RB, Bazylinski DA, Jannasch HW (1990b) Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343:258–260CrossRefGoogle Scholar
  198. Martins JL, Silveira TS, Silva KT, Lins U (2009) Salinity dependence of the distribution of multicellular magnetotactic prokaryotes in a hypersaline lagoon. Int Microbiol 12:193–201PubMedGoogle Scholar
  199. Maruyama K, Takeyama H, Nemoto E, Tanaka T, Yoda K, Matsunaga T (2004) Single nucleotide polymorphism detection in aldehyde dehydrogenase 2 (ALDH2) gene using bacterial magnetic particles based on dissociation curve analysis. Biotechnol Bioeng 87:687–694PubMedCrossRefGoogle Scholar
  200. Matsuda T, Endo J, Osakabe N, Tonomura A, Arii T (1983) Morphology and structure of biogenic magnetite. Nature 303:411–412CrossRefGoogle Scholar
  201. Matsunaga T (1991) Applications of bacterial magnets. Trends Biotechnol 9:91–95PubMedCrossRefGoogle Scholar
  202. Matsunaga T, Arakaki A (2007) Molecular bioengineering of bacterial magnetic particles for biotechnological applications. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, pp 227–254CrossRefGoogle Scholar
  203. Matsunaga T, Kamiya S (1987) Use of magnetic particles isolated from magnetotactic bacteria for enzyme immobilization. Appl Microbiol Biotechnol 26:328–332CrossRefGoogle Scholar
  204. Matsunaga T, Takeyama H (1998) Biomagnetic nanoparticle formation and application. Supramol Sci 5:391–394CrossRefGoogle Scholar
  205. Matsunaga T, Hashimoto K, Nakamura N, Nakamura K, Hashimoto S (1989) Phagocytosis of bacterial magnetite by leucocytes. Appl Microbiol Biotechnol 31:401–405CrossRefGoogle Scholar
  206. Matsunaga T, Tadokoro F, Nakamura N (1990) Mass culture of magnetic bacteria and their application to flow type immunoassays. IEEE Trans Magn 26:1557–1559CrossRefGoogle Scholar
  207. Matsunaga T, Nakamura C, Burgess JG, Sode K (1992) Gene-transfer in magnetic bacteria: transposon mutagenesis and cloning of genomic DNA fragments required for magnetosome synthesis. J Bacteriol 174:2748–2753PubMedGoogle Scholar
  208. Matsunaga T, Tsujimura N, Kamiya S (1996) Enhancement of magnetic particle production by nitrate and succinate fed-batch culture of Magnetospirillum sp. AMB-1. Biotechnol Tech 10:495–500CrossRefGoogle Scholar
  209. Matsunaga T, Higashi Y, Tsujimura N (1997) Drug delivery by magnetoliposomes containing bacterial magnetic particles. Cell Eng 2:7–11Google Scholar
  210. Matsunaga T, Sato R, Kamiya S, Tanaka T, Takeyama H (1999) Chemiluminescence enzyme immunoassay using protein A-bacterial magnetite complex. J Magn Magn Mater 194:126–131CrossRefGoogle Scholar
  211. Matsunaga T, Togo H, Kikuchi T, Tanaka T (2000a) Production of luciferase-magnetic particle complex by recombinant Magnetospirillum sp. AMB-1. Biotechnol Bioeng 70:704–709PubMedCrossRefGoogle Scholar
  212. Matsunaga T, Tsujimura N, Okamura Y, Takeyama H (2000b) Cloning and characterization of a gene, mpsA, encoding a protein associated with intracellular magnetic particles from Magnetospirillum sp. strain AMB-1. Biochem Biophys Res Commun 268:932–937PubMedCrossRefGoogle Scholar
  213. Matsunaga T, Arakaki A, Takahoko M (2002) Preparation of luciferase-bacterial magnetic particle complex by artificial integration of MagA-luciferase fusion protein into the bacterial magnetic particle membrane. Biotechnol Bioeng 77:614–618PubMedCrossRefGoogle Scholar
  214. Matsunaga T, Okamura Y, Fukuda Y, Wahyudi AT, Murase Y, Takeyama H (2005) Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res 12:157–166PubMedCrossRefGoogle Scholar
  215. Matsunaga T, Nemoto M, Arakaki A, Tanaka M (2009) Proteomic analysis of irregular, bullet-shaped magnetosomes in the sulphate-reducing magnetotactic bacterium Desulfovibrio magneticus RS-1. Proteomics 9:3341–3352PubMedCrossRefGoogle Scholar
  216. McAteer MA, Sibson NR, von Zur Muhlen C, Schneider JE, Lowe AS, Warrick N, Channon KM, Anthony DC, Choudhury RP (2007) In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat Med 13:1253–1258PubMedCrossRefGoogle Scholar
  217. McCartney MR, Lins U, Farina M, Buseck PR, Frankel RB (2001) Magnetic microstructure of bacterial magnetite by electron holography. Eur J Mineral 13:685–689CrossRefGoogle Scholar
  218. McKay DS, Gibson EK Jr, Thomas-Keprta KL, Vali H, Romanek CS, Clemett SJ, Chillier XD, Maechling CR, Zare RN (1996) Search for past life on mars: possible relic biogenic activity in martian meteorite ALH84001. Science 273:924–930PubMedCrossRefGoogle Scholar
  219. Meldrum FC, Heywood BR, Mann S, Frankel RB, Bazylinski DA (1993a) Electron microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium. Proc Roy Soc Lond B Bio 251:231–236CrossRefGoogle Scholar
  220. Meldrum FC, Heywood BR, Mann S, Frankel RB, Bazylinski DA (1993b) Electron microscopy study of magnetosomes in two cultured vibroid magnetotactic bacteria. Proc Roy Soc Lond B Bio 251:237–242CrossRefGoogle Scholar
  221. Moench TT (1988) Bilophococcus magnetotacticus gen. nov. sp. nov., a motile, magnetic coccus. Antonie Van Leeuwenhoek 54:483–496PubMedCrossRefGoogle Scholar
  222. Moench TT, Konetzka WA (1978) A novel method for the isolation and study of a magnetotactic bacterium. Arch Microbiol 119:203–212PubMedCrossRefGoogle Scholar
  223. Moskowitz BM, Bazylinski DA, Egli R, Frankel RB, Edwards KJ (2008) Magnetic properties of marine magnetotactic bacteria in a seasonally stratified coastal pond (Salt Pond, MA, USA). Geophys J Int 174:75–92CrossRefGoogle Scholar
  224. Murat D, Quinlan A, Vali H, Komeili A (2010) Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc Natl Acad Sci USA 107:5593–5598PubMedCrossRefGoogle Scholar
  225. Nakamura N, Matsunaga T (1993) Highly sensitive detection of allergen using bacterial magnetic particles. Anal Chim Acta 281:585–589CrossRefGoogle Scholar
  226. Nakamura N, Hashimoto K, Matsunaga T (1991) Immunoassay method for the determination of immunoglobulin G using bacterial magnetic particles. Anal Chem 63:268–272PubMedCrossRefGoogle Scholar
  227. Nakamura N, Burgess JG, Yagiuda K, Kudo S, Sakaguchi T, Matsunaga T (1993) Detection and removal of Escherichia coli using fluorescein isothiocyanate conjugated monoclonal antibody immobilized on bacterial magnetic particles. Anal Chem 65:2036–2039PubMedCrossRefGoogle Scholar
  228. Nakamura C, Burgess JG, Sode K, Matsunaga T (1995a) An iron-regulated gene, magA, encoding an iron transport protein of Magnetospirillum sp. strain AMB-1. J Biol Chem 270:28392–28396PubMedCrossRefGoogle Scholar
  229. Nakamura C, Kikuchi T, Burgess JG, Matsunaga T (1995b) Iron-regulated expression and membrane localization of the MagA protein in Magnetospirillum sp. strain AMB-1. J Biochem 118:23–27PubMedGoogle Scholar
  230. Nakayama H, Arakaki H, Maruyama K, Takeyama H, Matsunaga T (2003) Single-nucleotide polymorphism analysis using fluorescence resonance energy transfer between DNA-labeling fluorophore, fluorescein isothiocyanate, and DNA intercalator, POPO-3, on bacterial magnetic particles. Biotechnol Bioeng 84:96–102PubMedCrossRefGoogle Scholar
  231. Nakazawa H, Arakaki A, Narita-Yamada S, Yashiro I, Jinno K, Aoki N, Tsuruyama A, Okamura Y, Tanikawa S, Fujita N, Takeyama H, Matsunaga T (2009) Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria. Genome Res 19:1801–1808PubMedCrossRefGoogle Scholar
  232. Neilands JB (1984) A brief history of iron metabolism. Biol Metals 4:1–6CrossRefGoogle Scholar
  233. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  234. Nelson DC, Jannasch HW (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136:262–269CrossRefGoogle Scholar
  235. Ohuchi S, Schüler D (2009) In vivo display of a multisubunit enzyme complex on biogenic magnetic nanoparticles. Appl Environ Microbiol 75:7734–7738PubMedCrossRefGoogle Scholar
  236. Okamura Y, Takeyama H, Matsunaga T (2000) Two-dimensional analysis of proteins specific to the bacterial magnetic particle membrane from Magnetospirillum sp. AMB-1. Appl Biochem Biotechnol 84–86:441–446PubMedCrossRefGoogle Scholar
  237. Okamura Y, Takeyama H, Matsunaga T (2001) A magnetosome-specific GTPase from the magnetic bacterium Magnetospirillum magneticum AMB-1. J Biol Chem 276:48183–48188PubMedCrossRefGoogle Scholar
  238. Okamura Y, Takeyama H, Sekine T, Sakaguchi T, Wahyudi AT, Sato R, Kamiya S, Matsunaga T (2003) Design and application of a new cryptic-plasmid-based shuttle vector for Magnetospirillum magneticum. Appl Environ Microbiol 69:4274–4277PubMedCrossRefGoogle Scholar
  239. Okuda Y, Fukumori Y (2001) Expression and characterization of a magnetosome-associated protein, TPR-containing Mam22, in Escherichia coli. FEBS Lett 491:169–173PubMedCrossRefGoogle Scholar
  240. Okuda Y, Denda K, Fukumori Y (1996) Cloning and sequencing of a gene encoding a new member of the tetratricopeptide protein family from magnetosomes of Magnetospirillum magnetotacticum. Gene 171:99–102PubMedCrossRefGoogle Scholar
  241. Oldfield F, Wu RJ (2000) The magnetic properties of the recent sediments of Brothers Water, NW England. J Paleolimnol 23:165–174CrossRefGoogle Scholar
  242. Ota H, Takeyama H, Nakayama H, Katoh T, Matsunaga T (2003) SNP detection in transforming growth factor-beta1 gene using bacterial magnetic particles. Biosens Bioelectron 18:683–687PubMedCrossRefGoogle Scholar
  243. Palache C, Berman H, Frondel C (1944) Dana’s system of mineralogy. Wiley, New York, 384Google Scholar
  244. Pallen MJ, Wren BW (1997) The HtrA family of serine proteases. Mol Microbiol 26:209–221PubMedCrossRefGoogle Scholar
  245. Pan Y, Petersen N, Davila AF, Zhang L, Winklhofer M, Liu Q, Hanzlik M, Zhu R (2005) The detection of bacterial magnetite in recent sediments of Lake Chiemsee (southern Germany). Earth Planet Sci Lett 232:109–123CrossRefGoogle Scholar
  246. Paoletti LC, Blakemore RP (1986) Hydroxamate production by Aquaspirillum magnetotacticum. J Bacteriol 167:73–76PubMedGoogle Scholar
  247. Paulsen IT, Park JH, Choi PS, Saier MH Jr (1997) A family of Gram-negative bacterial outer membrane factors that function in the export of proteins,carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Lett 156:1–8PubMedCrossRefGoogle Scholar
  248. Penninga I, de Waard H, Moskowitz BM, Bazylinski DA, Frankel RB (1995) Remanence curves for individual magnetotactic bacteria using a pulsed magnetic field. J Magn Magn Mater 149:279–286CrossRefGoogle Scholar
  249. Perantoni M, Esquivel DM, Wajnberg E, Acosta-Avalos D, Cernicchiaro G, Lins de Barros H (2009) Magnetic properties of the microorganism Candidatus Magnetoglobus multicellularis. Naturwissenschaften 96:685–690PubMedCrossRefGoogle Scholar
  250. Petersen N, von Dobeneck T, Vali H (1986) Fossil bacterial magnetite in deep-sea sediments from the South Atlantic Ocean. Nature 320:611–615CrossRefGoogle Scholar
  251. Petersen N, Weiss DG, Vali H (1989) Magnetic bacteria in lake sediments. In: Lowes FJ, Collinson DW, Parry JH, Runcorn SK, Tozer DC, Soward A (eds) Geomagnetism and paleomagnetism. Kluwer Academic, Dordrecht, pp 231–241CrossRefGoogle Scholar
  252. Pikuta EV, Hoover RB, Bej AK, Marsic D, Whitman WB, Cleland D, Krader P (2003) Desulfonatronum thiodismutans sp. nov., a novel alkaliphilic, sulfate-reducing bacterium capable of lithoautotrophic growth. Int J Syst Evol Microbiol 53:1327–1332PubMedCrossRefGoogle Scholar
  253. Pollithy A, Romer T, Lang C, Müller FD, Helma J, Leonhardt H, Rothbauer U, Schüler D (2011) Magnetosome expression of functional camelid antibody fragments (nanobodies) in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 77:6165–6171PubMedCrossRefGoogle Scholar
  254. Ponting CC, Phillips C (1996) Rapsyn’s knobs and holes: eight tetratrico peptide repeats. Biochem J 314:1053–1054PubMedGoogle Scholar
  255. Pósfai M, Buseck PR, Bazylinski DA, Frankel RB (1998a) Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science 280:880–883PubMedCrossRefGoogle Scholar
  256. Pósfai M, Buseck PR, Bazylinski DA, Frankel RB (1998b) Iron sulfides from magnetotactic bacteria: structure, compositions, and phase transitions. Am Mineral 83:1469–1481Google Scholar
  257. Pósfai M, Cziner K, Marton E, Marton P, Buseck PR, Frankel RB, Bazylinski DA (2001) Crystal-size distributions and possible biogenic origin of Fe sulfides. Eur J Mineral 13:691–703CrossRefGoogle Scholar
  258. Pósfai M, Moskowitz BM, Arató B, Schüler D, Flies C, Bazylinski DA, Frankel RB (2006) Properties of intracellular magnetite crystals produced by Desulfovibrio magneticus strain RS-1. Earth Planet Sci Lett 249:444–455CrossRefGoogle Scholar
  259. Pradel N, Santini CL, Bernadac A, Fukumori Y, Wu LF (2006) Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proc Natl Acad Sci USA 103:17485–17489PubMedCrossRefGoogle Scholar
  260. Proksch RB, Moskowitz BM, Dahlberg ED, Schaeffer T, Bazylinski DA, Frankel RB (1995) Magnetic force microscopy of the submicron magnetic assembly in a magnetotactic bacterium. Appl Phys Lett 66:2582–2584CrossRefGoogle Scholar
  261. Prozorov T, Mallapragada SK, Narasimhan B, Wang L, Palo P, Nilsen-Hamilton M, Williams TJ, Bazylinski DA, Prozorov R, Canfield PC (2007) Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv Funct Mater 17:951–957CrossRefGoogle Scholar
  262. Qi L, Li J, Zhang W, Liu J, Rong C, Li Y, Wu L (2012) Fur in Magnetospirillum gryphiswaldense influences magnetosomes formation and directly regulates the genes involved in iron and oxygen metabolism. PLoS One 7:e29572PubMedCrossRefGoogle Scholar
  263. Quinlan A, Murat D, Vali H, Komeili A (2011) The HtrA/DegP family protease MamE is a bifunctional protein with roles in magnetosome protein localization and magnetite biomineralization. Mol Microbiol 80:1075–1087PubMedCrossRefGoogle Scholar
  264. Reiter WD, Palm P (1990) Identification and characterization of a defective SSV1 genome integrated into a tRNA gene in the archaebacterium Sulfolobus sp. B12. Mol Gen Genet 221:65–71PubMedCrossRefGoogle Scholar
  265. Richter M, Kube M, Bazylinski DA, Lombardot T, Reinhardt R, Glockner FO, Schüler D (2007) Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group specific genes with putative functions in magnetosome biomineralization and magnetotaxis. J Bacteriol 189:4899–4910PubMedCrossRefGoogle Scholar
  266. Rioux JB, Philippe N, Pereira S, Pignol D, Wu LF, Ginet N (2010) A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island. PLoS One 5:e9151PubMedCrossRefGoogle Scholar
  267. Rodgers FG, Blakemore RP, Blakemore NA, Frankel RB, Bazylinski DA, Maratea D, Rodgers C (1990a) Intercellular structure in a many-celled magnetotactic prokaryote. Arch Microbiol 145:18–22Google Scholar
  268. Rodgers FG, Blakemore RP, Blakemore NA, Frankel RB, Bazylinski DA, Maratea D, Rodgers C (1990b) Intercellular junctions, motility and magnetosome structure in a multicellular magnetotactic prokaryote. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum, New York, pp 231–237Google Scholar
  269. Sakaguchi T, Burgess JG, Matsunaga T (1993) Magnetite formation by a sulphate-reducing bacterium. Nature 365:47–49CrossRefGoogle Scholar
  270. Sakaguchi T, Arakaki A, Matsunaga T (2002) Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. Int J Syst Evol Microbiol 52:215–221PubMedGoogle Scholar
  271. Scheffel A, Schüler D (2007) The acidic repetitive domain of the Magnetospirillum gryphiswaldense MamJ protein displays hypervariability but is not required for magnetosome chain assembly. J Bacteriol 189:6437–6446PubMedCrossRefGoogle Scholar
  272. Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM, Schüler D (2006) An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440:110–114PubMedCrossRefGoogle Scholar
  273. Scheffel A, Gärdes A, Grünberg K, Wanner G, Schüler D (2008) The major magnetosome proteins MamGFDC are not essential for magnetite biomineralization in Magnetospirillum gryphiswaldense but regulate the size of magnetosome crystals. J Bacteriol 190:377–386PubMedCrossRefGoogle Scholar
  274. Schleifer K-H, Schüler D, Spring S, Weizenegger M, Amann R, Ludwig W, Kohler M (1991) The genus Magnetospirillum gen. nov., description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. Syst Appl Microbiol 14:379–385CrossRefGoogle Scholar
  275. Schübbe S, Kube M, Scheffel A, Wawer C, Heyen U, Meyerdierks A, Madkour MH, Mayer F, Reinhardt R, Schüler D (2003) Characterization of a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J Bacteriol 185:5779–5790PubMedCrossRefGoogle Scholar
  276. Schübbe S, Würdemann C, Peplies J, Heyen U, Wawer C, Glöckner FO, Schüler D (2006) Transcriptional organization and regulation of magnetosome operons in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 72:5757–5765PubMedCrossRefGoogle Scholar
  277. Schübbe S, Williams TJ, Xie G, Kiss HE, Brettin TS, Martinez D, Ross CA, Schüler D, Cox BL, Nealson KH, Bazylinski DA (2009) Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 75:4835–4852PubMedCrossRefGoogle Scholar
  278. Schüler D (2002) The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int Microbiol 5:209–214PubMedCrossRefGoogle Scholar
  279. Schüler D (2008) Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiol Rev 32:654–672PubMedCrossRefGoogle Scholar
  280. Schüler D, Baeuerlein E (1996) Iron-limited growth and kinetics of iron uptake in Magnetospirillum gryphiswaldense. Arch Microbiol 166:301–307PubMedCrossRefGoogle Scholar
  281. Schüler D, Baeuerlein E (1997) Iron transport and magnetite crystal formation of the magnetic bacterium Magnetospirillum gryphiswaldense. J Phys IV 7:647–650Google Scholar
  282. Schüler D, Baeuerlein E (1998) Dynamics of iron uptake and Fe3O4 mineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180:159–162PubMedGoogle Scholar
  283. Schüler D, Uhl R, Baeuerlein E (1995) A simple light-scattering method to assay magnetism in Magnetospirillum gryphiswaldense. FEMS Microbiol Lett 132:139–145CrossRefGoogle Scholar
  284. Schüler D, Spring S, Bazylinski DA (1999) Improved technique for the isolation of magnetotactic spirilla from a freshwater sediment and their phylogenetic characterization. Syst Appl Microbiol 22:466–471PubMedCrossRefGoogle Scholar
  285. Schultheiss D, Schüler D (2003) Development of a genetic system for Magnetospirillum gryphiswaldense. Arch Microbiol 179:89–94PubMedGoogle Scholar
  286. Schultheiss D, Kube M, Schüler D (2004) Inactivation of the flagellin gene flaA in Magnetospirillum gryphiswaldense results in nonmagnetotactic mutants lacking flagellar filaments. Appl Environ Microbiol 70:3624–3631PubMedCrossRefGoogle Scholar
  287. Schultheiss D, Handrick R, Jendrossek D, Hanzlik M, Schüler D (2005) The presumptive magnetosome protein Mms16 is a PHB-granule bound protein (phasin) in Magnetospirillum gryphiswaldense. J Bacteriol 187:2416–2425PubMedCrossRefGoogle Scholar
  288. Shapiro OH, Hatzenpichler R, Buckley DH, Zinder SH, Orphan VJ (2011) Multicellular photo-magnetotactic bacteria. Env Microbiol Rep 3:233–238CrossRefGoogle Scholar
  289. Silva KT, Abreu F, Almeida FP, Keim CN, Farina M, Lins U (2007) Flagellar apparatus of south seeking many celled magnetotactic prokaryotes. Microsc Res Tech 70:10–17PubMedCrossRefGoogle Scholar
  290. Simmons SL, Edwards KJ (2007) Unexpected diversity in populations of the many-celled magnetotactic prokaryote. Environ Microbiol 9:206–215PubMedCrossRefGoogle Scholar
  291. Simmons SL, Sievert SM, Frankel RB, Bazylinski DA, Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 70:6230–6239PubMedCrossRefGoogle Scholar
  292. Simmons SL, Bazylinski DA, Edwards KJ (2006) South seeking magnetotactic bacteria in the Northern Hemisphere. Science 311:371–374PubMedCrossRefGoogle Scholar
  293. Snowball IF (1991) Magnetic hysteresis properties of greigite (Fe3S4) and a new occurrence in Holocene sediments for Swedish Lappland. Phys Earth Planet Inter 68:32–40CrossRefGoogle Scholar
  294. Snowball IF (1994) Bacterial magnetite and the magnetic properties of sediments in a Swedish lake. Earth Planet Sci Lett 126:129–142CrossRefGoogle Scholar
  295. Snowball IF, Thompson R (1988) The occurrence of greigite in sediments from Loch Lomond. J Quat Sci 3:121–125CrossRefGoogle Scholar
  296. Snowball I, Zillen L, Sandgren P (2002) Bacterial magnetite in Swedish varved lake sediments: a potential bio marker of environmental change. Quat Int 88:13–19CrossRefGoogle Scholar
  297. Sode K, Kudo S, Sakaguchi T, Nakamura N, Matsunaga T (1993) Application of bacterial magnetic particles for highly selective messenger-RNA recovery system. Biotechnol Tech 7:688–694CrossRefGoogle Scholar
  298. Spormann AM, Wolfe RS (1984) Chemotactic, magnetotactic, and tactile behaviour in a magnetic spirillum. FEMS Microbiol Lett 22:171–177CrossRefGoogle Scholar
  299. Spring S, Amann R, Ludwig W, Schleifer KH, Petersen N (1992) Phylogenetic diversity and identification of nonculturable magnetotactic bacteria. Syst Appl Microbiol 15:116–122CrossRefGoogle Scholar
  300. Spring S, Amann R, Ludwig W, Schleifer KH, van Gemerden H, Petersen N (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microbiol 59:2397–2403PubMedGoogle Scholar
  301. Spring S, Amann R, Ludwig W, Schleifer KH, Schüler D, Poralla K, Petersen N (1994) Phylogenetic analysis of uncultured magnetotactic bacteria from the alpha-subclass of proteobacteria. Syst Appl Microbiol 17:501–508CrossRefGoogle Scholar
  302. Spring S, Lins U, Amann R, Schleifer KH, Ferreira LCS, Esquivel DMS, Farina M (1998) Phylogenetic affiliation and ultrastructure of uncultured magnetic bacteria with unusually large magnetosomes. Arch Microbiol 169:136–147PubMedCrossRefGoogle Scholar
  303. Staniland S, Williams W, Telling N, Van Der Laan G, Harrison A, Ward B (2008) Controlled cobalt doping of magnetosomes in vivo. Nat Nanotechnol 3:158–162PubMedCrossRefGoogle Scholar
  304. Stolz JF (1993) Magnetosomes. J Gen Microbiol 139:1663–1670CrossRefGoogle Scholar
  305. Stolz JF, Chang SBR, Kirschvink JL (1986) Magnetotactic bacteria and single-domain magnetite in hemipelagic sediments. Nature 321:849–851CrossRefGoogle Scholar
  306. Stolz JF, Lovley DR, Haggerty SE (1990) Biogenic magnetite and the magnetization of sediments. J Geophys Res 95:4355–4361CrossRefGoogle Scholar
  307. Sun JB, Duan JH, Dai SL, Ren J, Zhang YD, Tian JS, Li Y (2007) In vitro and in vivo antitumor effects of doxorubicin loaded with bacterial magnetosomes (DBMs) on H22 cells: the magnetic bio-nanoparticles as drug carriers. Cancer Lett 258:109–117PubMedCrossRefGoogle Scholar
  308. Sun JB, Zhao F, Tang T, Jiang W, Tian JS, Li Y, Li JL (2008) High-yield growth and magnetosome formation by Magnetospirillum gryphiswaldense MSR-1 in an oxygen-controlled fermenter supplied solely with air. Appl Microbiol Biotechnol 79:389–397PubMedCrossRefGoogle Scholar
  309. Suzuki H, Tanaka T, Sasaki T, Nakamura N, Matsunaga T, Mashiko S (1998) High resolution magnetic force microscope images of a magnetic particle chain extracted from magnetic bacteria AMB-1. Jpn J Appl Physiol 37:L1343–L1345CrossRefGoogle Scholar
  310. Suzuki T, Okamura Y, Calugay RJ, Takeyama H, Matsunaga T (2006) Global gene expression analysis of iron-inducible genes in Magnetospirillum magneticum AMB-1. J Bacteriol 188:2275–2279PubMedCrossRefGoogle Scholar
  311. Tanaka T, Maruyama K, Yoda K, Nemoto E, Udagawa Y, Nakayama H, Takeyama H, Matsunaga T (2003) Development and evaluation of an automated workstation for single nucleotide polymorphism discrimination using bacterial magnetic particles. Biosens Bioelectron 19:325–330PubMedCrossRefGoogle Scholar
  312. Tanaka M, Okamura Y, Arakaki A, Tanaka T, Takeyama H, Matsunaga T (2006) Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6:5234–5247PubMedCrossRefGoogle Scholar
  313. Taoka A, Asada R, Sasaki H, Anzawa K, Wu LF, Fukumori Y (2006) Spatial localizations of Mam22 and Mam12 in the magnetosomes of Magnetospirillum magnetotacticum. J Bacteriol 188:3805–3812PubMedCrossRefGoogle Scholar
  314. Thomas-Keprta KL, Bazylinski DA, Kirschvink JL, Clemett SJ, McKay DS, Wentworth SJ, Vali H, Gibson EK Jr, Romanek CS (2000) Elongated prismatic magnetite crystals in ALH84001 carbonate globules: potential Martian magnetofossils. Geochim Cosmochim Acta 64:4049–4081PubMedCrossRefGoogle Scholar
  315. Thomas-Keprta KL, Clemett SJ, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson EK Jr, McKay MF, Romanek CS (2001) Truncated hexa-octahedral magnetite crystals in ALH84001: presumptive biosignatures. Proc Natl Acad Sci USA 98:2164–2169PubMedCrossRefGoogle Scholar
  316. Thomas-Keprta KL, Clemett SJ, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson EK Jr, Romanek CS (2002) Magnetofossils from ancient Mars: a robust biosignature in the martian meteorite ALH84001. Appl Environ Microbiol 68:3663–3672PubMedCrossRefGoogle Scholar
  317. Thornhill RH, Burgess JG, Sakaguchi T, Matsunaga T (1994) A morphological classification of bacteria containing bullet-shaped magnetic particles. FEMS Microbiol Lett 115:169–176CrossRefGoogle Scholar
  318. Towe KM, Moench TT (1981) Electron-optical characterization of bacterial magnetite. Earth Planet Sci Lett 52:213–220CrossRefGoogle Scholar
  319. Uebe R, Voigt B, Schweder T, Albrecht D, Katzmann E, Lang C, Böttger L, Matzanke B, Schüler D (2010) Deletion of a fur-like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense. J Bacteriol 192:4192–4204PubMedCrossRefGoogle Scholar
  320. Uebe R, Henn V, Schüler D (2012) The MagA protein of magnetospirilla is not involved in bacterial magnetite biomineralization. J Bacteriol 194:1018–1023PubMedCrossRefGoogle Scholar
  321. Ullrich S, Schüler D (2010) Cre-lox-based method for generation of large deletions within the genomic magnetosome island of Magnetospirillum gryphiswaldense. Appl Environ Microbiol 76:2439–2444PubMedCrossRefGoogle Scholar
  322. Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D (2005) A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J Bacteriol 187:7176–7184PubMedCrossRefGoogle Scholar
  323. Vali H, Kirschvink JL (1989) Magnetofossil dissolution in a palaeomagnetically unstable deep‐sea sediment. Nature 339:203–206CrossRefGoogle Scholar
  324. Vali H, Forster O, Amarantidis G, Petersen N (1987) Magnetotactic bacteria and their magnetofossils in sediments. Earth Planet Sci Lett 86:389–400CrossRefGoogle Scholar
  325. Verosub KL, Roberts AP (1995) Environmental magnetism: past, present, and future. J Geophys Res 100:2175–2192CrossRefGoogle Scholar
  326. Weiss BP, Kim SS, Kirschvink JL, Kopp RE, Sankaran M, Kobayashi A, Komeili A (2004) Magnetic tests magnetosome chains in Martian meteorite ALH84001. Proc Natl Acad Sci USA 101:8281–8284PubMedCrossRefGoogle Scholar
  327. Wenter R, Wanner G, Schüler D, Overmann J (2009) Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments. Environ Microbiol 11:1493–1505PubMedCrossRefGoogle Scholar
  328. Williams TJ, Zhang CL, Scott JH, Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 72:1322–1329PubMedCrossRefGoogle Scholar
  329. Williams TJ, Lefèvre CT, Zhao W, Beveridge TJ, Bazylinski DA (2012) Magnetospira thiophila, gen. nov. sp. nov., a new marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae (Alphaproteobacteria). Int J Syst Evol Microbiol 62:2443–2450Google Scholar
  330. Winklhofer M, Abraçado LG, Davila AF, Keim CN, Lins de Barros HGP (2007) Magnetic optimization in a multicellular magnetotactic organism. Biophys J 92:661–670PubMedCrossRefGoogle Scholar
  331. Wolfe RS, Thauer RK, Pfennig N (1987) A capillary racetrack method for isolation of magnetotactic bacteria. FEMS Microbiol Lett 45:31–35CrossRefGoogle Scholar
  332. Xiang L, Wei J, Jianbo S, Guili W, Feng G, Ying L (2007) Purified and sterilized magnetosomes from Magnetospirillum gryphiswaldense MSR-1 were not toxic to mouse fibroblasts in vitro. Lett Appl Microbiol 45:75–81PubMedCrossRefGoogle Scholar
  333. Xie J, Chen K, Chen X (2009) Production, modification and bio-applications of magnetic nanoparticles gestated by magnetotactic bacteria. Nano Res 2:261–278PubMedCrossRefGoogle Scholar
  334. Yang CD, Takeyama H, Tanaka T, Hasegawa A, Matsunaga T (2001a) Synthesis of bacterial magnetic particles during cell cycle of Magnetospirillum magneticum AMB-1. Appl Biochem Biotechnol 91–93:155–160PubMedCrossRefGoogle Scholar
  335. Yang C, Takeyama H, Tanaka T, Matsunaga T (2001b) Effects of growth medium composition, iron sources and atmospheric oxygen concentrations on production of luciferase-bacterial magnetic particle complex by a recombinant Magnetospirillum magneticum AMB-1. Enzyme Microb Technol 29:13–19PubMedCrossRefGoogle Scholar
  336. Yang W, Li R, Peng T, Zhang Y, Jiang W, Li Y, Li J (2010) mamO and mamE genes are essential for magnetosome crystal biomineralization in Magnetospirillum gryphiswaldense MSR-1. Res Microbiol 161:701–705PubMedCrossRefGoogle Scholar
  337. Yoshino T, Matsunaga T (2005) Development of efficient expression system for protein display on bacterial magnetic particles. Biochem Biophys Res Commun 338:1678–1681PubMedCrossRefGoogle Scholar
  338. Yoshino T, Matsunaga T (2006) Efficient and stable display of functional proteins on bacterial magnetic particles using Mms13 as a novel anchor molecule. Appl Environ Microbiol 72:465–471PubMedCrossRefGoogle Scholar
  339. Yoshino T, Tanaka T, Takeyama H, Matsunaga T (2003) Single nucleotide polymorphism genotyping of aldehyde dehydrogenase 2 gene using a single bacterial magnetic particle. Biosens Bioelectron 18:661–666PubMedCrossRefGoogle Scholar
  340. Yoza B, Matsumoto M, Matsunaga T (2002) DNA extraction using modified bacterial magnetic particles in the presence of amino silane compound. J Biotechnol 94:217–224PubMedCrossRefGoogle Scholar
  341. Yoza B, Arakaki A, Maruyama K, Takeyama H, Matsunaga T (2003a) Fully automated DNA extraction from blood using magnetic particles modified with a hyperbranched polyamidoamine dendrimer. J Biosci Bioeng 95:21–26PubMedGoogle Scholar
  342. Yoza B, Arakaki A, Matsunaga T (2003b) DNA extraction using bacterial magnetic particles modified with hyperbranched polyamidoamine dendrimer. J Biotechnol 101:219–228PubMedCrossRefGoogle Scholar
  343. Zhao L, Wu D, Wu L-F, Song T (2007) A simple and accurate method for quantification of magnetosomes in magnetotactic bacteria by common spectrophotometer. J Biochem Biophys Methods 70:377–383PubMedCrossRefGoogle Scholar
  344. Zhao M, Lliang C, Li A, Chang J, Wang H, Yan R, Zhang J, Tai J (2010) Magnetic paclitaxel nanoparticles inhibit glioma growth and improve the survival of rats bearing glioma xenografts. Anticancer Res 30:2217–2223PubMedGoogle Scholar
  345. Zhou K, Pan H, Zhang S, Yue H, Xiao T, Wu L (2011) Occurrence and microscopic analysis of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea. Chin J Oceanol Limn 29:246–251CrossRefGoogle Scholar
  346. Zhou K, Zhang WY, Yu-Zhang K, Pan HM, Zhang SD, Zhang WJ, Yue HD, Li Y, Xiao T, Wu LF (2012) A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea. Environ Microbiol 14:405–413PubMedCrossRefGoogle Scholar
  347. Zhu K, Pan H, Li J, Yu-Zhang K, Zhang SD, Zhang WY, Zhou K, Yue H, Pan Y, Xiao T, Wu LF (2010) Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Res Microbiol 161:276–283PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Dennis A. Bazylinski
    • 1
    Email author
  • Christopher T. Lefèvre
    • 2
  • Dirk Schüler
    • 3
  1. 1.School of Life SciencesUniversity of Nevada at Las VegasLas VegasUSA
  2. 2.CEA Cadarache/CNRS/Université Aix-Marseille II, UMR7265 Service de Biologie Végétale et de Microbiologie EnvironnementaleLaboratoire de Bioénergétique CellulaireSaint Paul lez DuranceFrance
  3. 3.Department Biologie ILudwig-Maximilians-Universität MünchenPlanegg-MartinsriedGermany

Personalised recommendations