Abstract
The ability of magnetotactic bacteria (MTB) to orient and migrate along magnetic field lines is basedon magnetosomes, which are membrane-enclosed intracellular crystals of a magnetic iron mineral. Thebiomineralization of magnetosomes is a process with genetic control over the accumulation of iron,the deposition of the magnetic crystal within a specific compartment, as well as their intracellularassembly and alignment into chain-like structures. Magnetite crystals produced by MTB have uniform species-specificmorphologies and sizes, which are mostly unknown from inorganic systems. In addition, magnetosome chainformation is an example of the highest structural level achievable in a prokaryotic cell. In thiswork, we give an overview of the biology of MTB and the structure and functions of bacterial magnetosomes.In addition we summarize the current knowledge of the physico-chemical and molecular genetic basis of magnetosomebiomineralization and chain formation.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
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 278:8745–8750
Baeuerlein E (2003) Biomineralization of Unicellular Organisms: An Unusual Membrane Biochemistry for the Production of Inorganic Nano- and Microstructures. Angew Chem Int Ed 42:614–641
Balkwill D, Maratea D, Blakemore R (1980) Ultrastructure of a magnetotactic spirillum. J Bacteriol 141:1399–1408
Baumeister W, Grimm R, Walz J (1999) Electron tomography of molecules and cells. Trends in Cell Biology 9:81–85
Bazylinski DA, Heywood BR, Mann S, Frankel RB (1993) Fe3O4and FeS4in a bacterium. Nature 366:218
Bazylinski DA, Garratt-Reed A, Frankel RB (1994) Electron-microscopic studies of magnetosomes in magnetotactic bacteria. Microsc Res Tech 27:389–401
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 61:3232–3239
Bazylinski D (1998) Ultrastructure and function of the bacterial magnetosome. Abstracts of the General Meeting of the American Society for Microbiology 981998:15
Bazylinski DA, Dean AJ, Williams TJ, Long LK, Middleton SL, Dubbels BL (2004) Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 182:373–387
Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217–230
Blakemore R (1975) Magnetotactic bacteria. Science 190:377–379
Blakemore R, Maratea D, Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140:720–729
Blakemore RP, Short KA, Bazylinski DA, Rosenblatt C, Frankel RB (1985) Microaerobic conditions are required for magnetite formation within Aquaspirillum magnetotacticum. Geomicrobiol J 4:53–72
Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21:932–939
Calugay RJ, Miyashita H, Okamura Y, Matsunaga T (2003) Siderophore production by the magnetic bacterium Magnetospirillum magneticum AMB-1. FEMS Microbiol Lett 218:371–375
Calugay RJ, Okamura Y, Wahyudi AT, Takeyama H, Matsunaga T (2004) Siderophore production of a periplasmic transport binding protein kinase gene defective mutant of Magnetospirillum magneticum AMB-1. Biochem Biophys Res Commun 323:852–857
Clausen T, Southan C, Ehrmann M (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10:443–455
DeLong EF, Frankel RB, Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259:803–806
Devouard B, Posfai M, Hua X, Bazylinski DA, Frankel RB, Buseck PR (1998) Magnetite from magnetotactic bacteria: size distributions and twinning. Am Mineral 83:1387–1398
Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424
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 150:2931–2945
Dunin-Borkowski RE, McCartney MR, Frankel RB, Bazylinski DA, Posfai M, Buseck PR (1998) Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282:1868–1870
Dunin-Borkowski RE, McCartney MR, Posfai 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 13:671–684
Errington J (2003) Dynamic proteins and a cytoskeleton in bacteria. Nat Cell Biol 5:175–178
Faivre D, Arginier P, Menguy N, Zuddas P, Pachana K, Gloter A, Laval JY, Guyot F (2004) Mineralogical and isotopic properties of inorganic nanocrystalline magnetites. Geochim Cosmochim Acta 68:4395–4403
Farina M, Lins de Barros HGP, Esquivel DMS, Danon J (1983) Ultrastructure of a magnetotactic microorganism. Biology of the Cell 48:85–88
Farina M, Esquivel DMS, Lins de Barros HGP (1990) Magnetic iron-sulfur crystals from a magnetotactic microorganism. Nature 343:256–258
Flies C, Peplies J, Schüler D (2005a) A combined approach for the characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol 71:2723–2731
Flies C, Jonkers H, deBeer D, Bosselmann K, Böttcher M, Schüler D (2005b) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 52:185–195
Frankel RB, Papaefthymiou GC, Blakemore RP, O'Brien W (1983) Fe3O4precipitation in magnetotactic bacteria. Biochim Biophys Acta 763:147–159
Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73:994–1000
Gorby YA, Beveridge TJ, Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170:834–841
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 183:9–18
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 67:4573–4582
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 70:1040–1050
Guerin W, Blakemore R (1992) Redox cycling of iron supports growth and magnetite synthesis by Aquaspirillum magnetotacticum. Appl Environ Microbiol 58:1102–1109
Handrick R, Reinhardt S, Schultheiss D, Reichart T, Schüler D, Jendrossek V, Jendrossek D (2004) Unraveling the function of the Rhodospirillum rubrum activator of polyhydroxybutyrate (PHB) degradation: the activator is a PHB-granule-bound protein (phasin). J Bacteriol 186:2466–2475
Hanzlik M, Winklhofer M, Petersen N (2002) Pulsed-field-remanence measurements on individual magnetotactic bacteria. J Magn Magn Mater 248:258–267
Hergt R, Hiergeist R, Zeisberger M, Schüler D, Heyen U, Hilger I, Kaiser WA (2005) Magnetic properties of bacterial magnetosomes as diagnostic and therapeutic tools. J Magn Magn Mater 293:80–86
Heyen U, Schüler D (2003) Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl Microbiol Biotechnol 61:536–544
Kawaguchi R, Burgess JG, Sakaguchi T, Takeyama H, Thornhill RH, Matsunaga T (1995) Phylogenetic analysis of a novel sulfate-reducing magnetic bacterium, Rs-1, demonstrates its membership of the Delta-proteobacteria. FEMS Microbiol Lett 126:277–282
Kirschvink JL (1982) Paleomagnetic evidence for fossil biogenic magnetite in western Crete. Earth Planet Sci Lett 59:388–392
Kirschvink JL, Walker MM, Diebel CE (2001) Magnetite-based magnetoreception. Curr Opin Neurobiol 11:462–467
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 101:3839–3844
Komeili A, Li Z, Newman DK, Jensen GJ (2005) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Sciencexpress 10.1126/science.1123231
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 76:6207–6213
Lang C, Schüler D (2006) Biomineralization of magnetosomes in bacteria: nanoparticles with potential applications. In: Microbial bionanotechnology – biological self-assembly systems and biopolymer-based nanostructures, BHA Rehm, ed. (Wymondham, Horizon Bioscience), pp 107–124
Lins U, Farina M (1998) Magnetosome size distribution in uncultured rod-shaped bacteria as determined by electron microscopy and electron spectroscopic imaging. Microsc Res Tech 42:459–464
Mann S, Sparks NHC, Frankel RB, Bazylinski DA, Jannasch HW (1990a) Biomineralization of ferrimagnetic greigite (Fe3O4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343:258–260
Mann S, Sparks N, Board R (1990b) Magnetotactic bacteria: microbiology, biomineralization, palaeomagnetism and biotechnology. Adv Microb Physiol 31:125–181
Matsunaga T, Nakamura C, Burgess J, Sode S (1992) Gene transfer in magnetic bacteria: transposon mutagenesis and cloning of genomic DNA fragments required for magnetosome synthesis. J Bacteriol 174:2748–2753
Matsunaga T, Tsujimura N, Okamura H, Takeyama H (2000) 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 268:932–937
Matsunaga T, Okamura Y, Tanaka T (2004) Biotechnological application of nano-scale engineered bacterial magnetic particles. J Mater Chem 14:2099–2105
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 Research 12:157–166
Moench T (1988) Bilophococcus magnetotacticus gen nov sp nov, a motile, magnetic coccus. Antonie van Leeuwenhoek 54:483–496
Moskowitz BM (1995) Biomineralization of magnetic minerals. Rev Geophys 33:123–128
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339
Okamura Y, Takeyama H, Matsunaga T (2001) A magnetosome-specific GTPase from the magnetic bacterium Magnetospirillum magneticum AMB-1. J Biol Chem 276:48183–48188
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 171:99–102
Okuda Y, Fukumori Y (2001) Expression and characterization of a magnetosome-associated protein, TPR-containing MAM22, in Escherichia coli. FEBS Lett 491:169–173
Paoletti L, Blakemore R (1986) Hydroxamate produktion by Aquaspirillum magnetotacticum. J Bacteriol 167:153–163
Paulsen IT, Saier MH (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156:99–103
Philipse AP, Maas D (2002) Magnetic colloids from magnetotactic bacteria: Chain formation and colloidal stability. Langmuir 18:9977–9984
Posfai M, Buseck PR, Bazylinski DA, Frankel RB (1998a) Iron sulfides from magnetotactic bacteria: structure, composition, and phase transitions. Am Mineral 83:1469–1481
Posfai M, Buseck PR, Bazylinski DA, Frankel RB (1998b) Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science 280:880–883
Proksch RB, Schaffer TE, Moskowitz BM, Dahlberg ED, Bazylinski DA, Frankel RB (1995) Magnetic force microscopy of the submicron magnetic assembly in a magnetotactic bacterium. Appl Phys Lett 66:2582–2584
Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM, Schüler D (2005) An acidic protein aligns magnetosomes along a filamentous structure. Nature advance online publication 10.1038/nature04382
Schultheiss D, Schüler D (2003) Development of a genetic system for Magnetospirillum gryphiswaldense. Arch Microbiol 179:89–94
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 70:3624–3631
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 187:2416–2425
Schübbe S, Kube M, Scheffel A, Wawer C, Heyen U, Meyerdierks A, Madkour M, 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 185:5779–5790
Schüler D, Baeuerlein E (1996) Iron-limited growth and kinetics of iron uptake in Magnetospirillum gryphiswaldense. Arch Microbiol 166:301–307
Schüler D, Baeuerlein E (1998) Dynamics of iron uptake and Fe3O4biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180:159–162
Schüler D (1999) Formation of magnetosomes in magnetotactic bacteria. J Mol Microbiol Biotechnol 1:79–86
Schüler D, Frankel RB (1999) Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications. Appl Microbiol Biotechnol 52:464–473
Schüler D (2004) Molecular analysis of a subcellular compartment: The magnetosome membrane in Magnetospirillum gryphiswaldense. Arch Microbiol 181:1–7
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 70:6230–6239
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 7:688–694
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 59:2397–2403
Spring S, Amann R, Ludwig W, Schleifer K-H, Schüler D, Poralla K, Petersen N (1994) Phylogenetic analysis of uncultured magnetotactic bacteria from the alpha-subclass of Proteobacteria. Systematic & Applied Microbiology 17:501–508
Tanaka T, Matsunaga T (2000) Fully automated chemiluminescence immunoassay of insulin using antibody-protein A-bacterial magnetic particle complexes. Anal Biochem 72:3518–3522
Tanaka T, Takeda H, Ueki F, Obata K, Tajima H, Takeyama H, Goda Y, Fujimoto S, Matsunaga T (2004) Rapid and sensitive detection of 17 beta-estradiol in environmental water using automated immunoassay system with bacterial magnetic particles. J Biotechnol 108:153–159
Taylor AP, Barry JC (2004) Magnetosomal matrix: ultrafine structure may template biomineralization of magnetosomes. J Microsc (Oxf) 213:180–197
Thomas-Keprta KL, Clemett SJ, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson Jr. EK, Romanek CS (2002) Magnetofossils from ancient Mars: a robust biosignature in the martian meteorite ALH84001. Appl Environ Microbiol 68:3663–3672
Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D (2005) A hypervariable 130 kb genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island, which undergoes frequent rearrangements during stationary growth. J Bacteriol 187:7176–7184
Vali H, Forster O, Amarantidis G, Petersen N (1987) Magnetotactic bacteria and their magnetofossils in sediments. Earth Planetary Sci Lett 86:2–4
Wahyudi AT, Takeyama H, Matsunaga T (2001) Isolation of Magnetospirillum magneticum AMB-1 mutants defective in bacterial magnetic particle synthesis by transposon mutagenesis. Appl Biochem Biotechnol 91–93:147–154
Wahyudi AT, Takeyama H, Okamura Y, Fukuda Y, Matsunaga T (2003) Characterization of aldehyde ferredoxin oxidoreductase gene defective mutant in Magnetospirillum magneticum AMB-1. Biochem Biophys Res Commun 303:223–229
Williams TJ, Zhang CL, Scott JH, Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccis strain MC-1. Appl Environ Microbiol 72(2):1322–1329
Yamazaki T, Oyanagi H, Fujiwara T, Fukumori Y (1995) Nitrite reductase from the magnetotactic bacterium Magnetospirillum magnetotacticum – a novel cytochrome Cd(1) with Fe(II)-nitrite oxidoreductase activity. Eur J Biochem 233:665–671
Yoza B, Arakaki A, Matsunaga T (2003a) DNA extraction using bacterial magnetic particles modified with hyperbranched polyamidoamine dendrimer. J Biotechnol 101:219–228
Yoza B, Arakaki A, Maruyama K, Takeyama H, Matsunaga T (2003b) Fully automated DNA extraction from blood using magnetic particles modified with a hyperbranched polyamidoamine dendrimer. J Biosci Bioeng 95:21–26
Acknowledgments
We would like to acknowledge our students, colleagues, and numerous collaborators. Research in the authors lab is supported by the Max Planck Society, the Deutsche Forschungsgemeinschaft, and the German BMBF.
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
Copyright information
© 2006 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Scheffel, A., Schüler, D. (2006). Magnetosomes in Magnetotactic Bacteria. In: Shively, J.M. (eds) Complex Intracellular Structures in Prokaryotes. Microbiology Monographs, vol 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_024
Download citation
DOI: https://doi.org/10.1007/7171_024
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-32524-6
Online ISBN: 978-3-540-32526-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)