Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria

FEMS Microbiology Reviews

Volumn 36, Issue 1, 2012, Pages 232-255

  Komeili, Arash ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacterial organelle; Biomineralization; Compartmentalization; Magnetite; Magnetosome; Magnetotactic bacteria

Indexed keywords

BIOMINERALIZATION; CELL COMPARTMENTALIZATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; IRON TRANSPORT; MAGNETOSOME; NONHUMAN; PROTEIN TARGETING; REVIEW;

ALPHAPROTEOBACTERIA; CYTOSKELETON; DELTAPROTEOBACTERIA; FERUMOXYTOL; INTRACELLULAR MEMBRANES; IRON; LOCOMOTION; MAGNETOSOMES; METABOLIC NETWORKS AND PATHWAYS; PROTEIN TRANSPORT;

EID: 83355174257     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2011.00315.x     Document Type: Review

References (143)

1. Abreu F, Martins JL, Silveira TS, Keim CN, de Barros HG, Filho FJ & Lins U (2007) 'Candidatus Magnetoglobus multicellularis', a multicellular, magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol 57: 1318-1322.
2. Abreu FP, Silva KT, Farina M, Keim CN & Lins U (2008) Greigite magnetosome membrane ultrastructure in 'Candidatus Magnetoglobus multicellularis'. Int Microbiol 11: 75-80.
3. Abreu F, Cantao ME, Nicolas MF et al. (2011) Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria. ISME J 5: 1634-1640.
4. Alexandre G, Greer-Phillips S & Zhulin IB (2004) Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev 28: 113-126.
5. 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: 6279-6296.
6. Amemiya Y, Arakaki A, Staniland SS, Tanaka T & Matsunaga T (2007) Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6. Biomaterials 28: 5381-5389.
7. 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.
8. Arakaki A, Masuda F, Amemiya Y, Tanaka T & Matsunaga T (2010) Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from magnetotactic bacteria. J Colloid Interface Sci 343: 65-70.
9. Balkwill DL, Maratea D & Blakemore RP (1980) Ultrastructure of a magnetotactic spirillum. J Bacteriol 141: 1399-1408.
10. Bazylinski DA & Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2: 217-230.
11. Bazylinski DA, Garrattreed AJ, Abedi A & Frankel RB (1993) Copper association with iron sulfide magnetosomes in a magnetotactic bacterium. Arch Microbiol 160: 35-42.
12. 4) in a magnetotactic bacterium. Appl Environ Microbiol 61: 3232-3239.
13. Bellini S (2009a) Further studies on "magnetosensitive bacteria". Chin J Oceanol Limnol 27: 6-12.
14. Bellini S (2009b) On a unique behavior of freshwater bacteria. Chin J Oceanol Limnol 27: 3-5.
15. Blakemore R (1975) Magnetotactic bacteria. Science 190: 377-379.
16. Blakemore RP (1982) Magnetotactic bacteria. Annu Rev Microbiol 36: 217-238.
17. Blakemore RP, Maratea D & Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140: 720-729.
18. Blakemore RP, Frankel RB & Kalmijn AJ (1980) South-seeking magnetotactic bacteria in the Southern-Hemisphere. Nature 286: 384-385.
19. Blakemore RP, Short KA, Bazylinski DA, Rosenblatt C & Frankel RB (1985) Microaerobic conditions are required for magnetite formation within Aquaspirillum magnetotacticum. Geomicrobiol J 4: 53-71.
20. Bowman GR, Comolli LR, Zhu J et al. (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134: 945-955.
21. 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. P Natl Acad Sci USA 107: 12263-12268.
22. 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.
23. Carballido-Lopez R (2006) The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70: 888-909.
24. Chen C, Ma Q, Jiang W & Song T (2011) Phototaxis in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1 is independent of magnetic fields. Appl Microbiol Biotechnol 90: 269-275.
25. Delong EF, Frankel RB & Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259: 803-806.
26. 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: 534-552.
27. Ding Y, Li J, Liu J, Yang J, Jiang W, Tian J, Li Y & Pan Y (2010) Deletion of the ftsZ-like gene results in the production of superparamagnetic magnetite magnetosomes in Magnetospirillum gryphiswaldense. J Bacteriol 192: 1097-1105.
28. D'Orazio SE, Velasquez M, Roan NR, Naveiras-Torres O & Starnbach MN (2003) The Listeria monocytogenes lemA gene product is not required for intracellular infection or to activate fMIGWII-specific T cells. Infect Immun 71: 6721-6727.
29. 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: 342-354.
30. Ebersbach G, Briegel A, Jensen GJ & Jacobs-Wagner C (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in caulobacter. Cell 134: 956-968.
31. Faivre D, Böttger 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 Engl 46: 8495-8499.
32. Frankel RB (2009) The discovery of magnetotactic/magnetosensitive bacteria. Chin J Oceanol Limnol 27: 1-2.
33. Frankel RB & Blakemore RP (1980) Navigational compass in magnetic bacteria. J Magn Magn Mater 15-8: 1562-1564.
34. Frankel RB, Blakemore RP & Wolfe RS (1979) Magnetite in freshwater magnetotactic bacteria. Science 203: 1355-1356.
35. Frankel RB, Blakemore RP, De Araujo FF, Esquivel DM & Danon J (1981) Magnetotactic bacteria at the geomagnetic equator. Science 212: 1269-1270.
36. 4 precipitation in magnetotactic bacteria. Biochim Biophys Acta 763: 147-159.
37. Frankel RB, Bazylinski DA, Johnson MS & Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73: 994-1000.
38. 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: 801-812.
39. Gallop JL & McMahon HT (2005) BAR domains and membrane curvature: bringing your curves to the BAR. Biochem Soc Symp 438: 223-231.
40. Ge X, Wang K, Bo T, Kou Y, Liu W & Chen G (2011) Magnetospirillum magneticum AMB-1 peroxiredoxins contribute to the aerotolerance and genetic stability of the genomic magnetosome island. FEMS Microbiol Lett 320: 118-127.
41. Glasauer S, Langley S & Beveridge TJ (2002) Intracellular iron minerals in a dissimilatory iron-reducing bacterium. Science 295: 117-119.
42. Goldhawk DE, Lemaire C, McCreary CR, McGirr R, Dhanvantari S, Thompson RT, Figueredo R, Koropatnick J, Foster P & Prato FS (2009) Magnetic resonance imaging of cells overexpressing MagA, an endogenous contrast agent for live cell imaging. Mol Imaging 8: 129-139.
43. Gorby YA, Beveridge TJ & Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170: 834-841.
44. Graham TR & Kozlov MM (2010) Interplay of proteins and lipids in generating membrane curvature. Curr Opin Cell Biol 22: 430-436.
45. 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.
46. 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.
47. Hanzlik M, Winklhofer M & Petersen N (2002) Pulsed-field-remanence measurements on individual magnetotactic bacteria. J Magn Magn Mater 248: 258-267.
48. Hautot D, Pankhurst QA, Morris CM, Curtis A, Burn J & Dobson J (2007) Preliminary observation of elevated levels of nanocrystalline iron oxide in the basal ganglia of neuroferritinopathy patients. Biochim Biophys Acta 1772: 21-25.
49. Heyen U & Schüler D (2003) Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl Microbiol Biotechnol 61: 536-544.
50. Hildebrand M (2008) Diatoms, biomineralization processes, and genomics. Chem Rev 108: 4855-4874.
51. Hsu CY, Ko FY, Li CW, Fann K & Lue JT (2007) Magnetoreception system in honeybees (Apis mellifera). PLoS ONE 2: e395.
52. Ito A, Shinkai M, Honda H & Kobayashi T (2005) Medical application of functionalized magnetic nanoparticles. J Biosci Bioeng 100: 1-11.
53. Jogler C & Schüler D (2009) Genomics, genetics, and cell biology of magnetosome formation. Annu Rev Microbiol 63: 501-521.
54. Jogler C, Lin W, Meyerdierks A, Kube M, Katzmann E, Flies C, Pan Y, Amann R, Reinhardt R & Schüler D (2009) Towards cloning the magnetotactic metagenome: identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol 75: 3972-3979.
55. Jogler C, Niebler M, Lin W et al. (2010) Cultivation-independent characterization of 'Candidatus Magnetobacterium bavaricum' via ultrastructural, geochemical, ecological and metagenomic methods. Environ Microbiol 12: 2466-2478.
56. 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. P Natl Acad Sci USA 108: 1134-1139.
57. 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: 208-224.
58. Keim CN, Abreu F, Lins U, Lins de Barros H & Farina M (2004) Cell organization and ultrastructure of a magnetotactic multicellular organism. J Struct Biol 145: 254-262.
59. Keim CN, Lins U & Farina M (2009) Manganese in biogenic magnetite crystals from magnetotactic bacteria. FEMS Microbiol Lett 292: 250-253.
60. Kirschvink JL (1981) The horizontal magnetic dance of the honeybee is compatible with a single-domain ferromagnetic magnetoreceptor. Biosystems 14: 193-203.
61. Kirschvink JL & Gould JL (1981) Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 13: 181-201.
62. Kirschvink JL & Hagadorn JW (2000) A Grand Unified Theory of Biomineralization. (Bäuerlein E., ed.) The Biomineralisation of Nano- and Micro-Structures, Wiley-VCH Verlag GmbH, Weinheim, Germany, pp. 139-149.
63. Kirschvink JL, Kobayashi-Kirschvink A & Woodford BJ (1992) Magnetite biomineralization in the human brain. P Natl Acad Sci USA 89: 7683-7687.
64. Komeili A, Vali H, Beveridge TJ & Newman DK (2004) Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. P Natl Acad Sci USA 101: 3839-3844.
65. Komeili A, Li Z, Newman DK & Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311: 242-245.
66. Kopp RE & Kirschvink JL (2008) The identification and biogeochemical interpretation of fossil magnetotactic bacteria. Earth Sci Rev 86: 42-61.
67. Kröger N, Deutzmann R & Sumper M (1999) Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science 286: 1129-1132.
68. Kröger N, Deutzmann R, Bergsdorf C & Sumper M (2000) Species-specific polyamines from diatoms control silica morphology. P Natl Acad Sci USA 97: 14133-14138.
69. Lang C & Schüler D (2008) Expression of green fluorescent protein fused to magnetosome proteins in microaerophilic magnetotactic bacteria. Appl Environ Microbiol 74: 4944-4953.
70. 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: 144-151.
71. Lefèvre CT, Abreu F, Schmidt ML, Lins U, Frankel RB, Hedlund BP & Bazylinski DA (2010) Moderately thermophilic magnetotactic bacteria from hot springs in Nevada. Appl Environ Microbiol 76: 3740-3743.
72. 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: 538-549.
73. Lefèvre CT, Frankel RB, Pósfai M, Prozorov T & Bazylinski DA (2011b) Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ Microbiol 13: 2342-2350.
74. Mann S, Sparks NH, Walker MM & Kirschvink JL (1988) Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: implications for magnetoreception. J Exp Biol 140: 35-49.
75. 2) in a magnetotactic bacterium. Nature 343: 258-261.
76. Matsunaga T, Sakaguchi T & Tadokoro F (1991) Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol 35: 651-655.
77. 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: 2748-2753.
78. Matsunaga T, Tsujimura N, Okamura Y & 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.
79. 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: 157-166.
80. 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: 3341-3352.
81. Meldrum FC, Mann S, Heywood BR, Frankel RB & Bazylinski DA (1993) Electron-microscopy study of magnetosomes in 2 cultured vibrioid magnetotactic bacteria. Proc R Soc Lond B Biol Sci 251: 237-242.
82. Mikhaylova A, Davidson M, Toastmann H, Channell JE, Guyodo Y, Batich C & Dobson J (2005) Detection, identification and mapping of iron anomalies in brain tissue using X-ray absorption spectroscopy. J R Soc Interface 2: 33-37.
83. Murat D, Byrne M & Komeili A (2010a) Cell biology of prokaryotic organelles. Cold Spring Harb Perspect Biol 2: a000422.
84. Murat D, Quinlan A, Vali H & Komeili A (2010b) Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. P Natl Acad Sci USA 107: 5593-5598.
85. 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: 28392-28396.
86. 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: 23-27.
87. Nakazawa H, Arakaki A, Narita-Yamada S et al. (2009) Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria. Genome Res 19: 1801-1808.
88. 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.
89. Okuda Y & Fukumori Y (2001) Expression and characterization of a magnetosome-associated protein, TPR-containing MAM22, in Escherichia coli. FEBS Lett 491: 169-173.
90. 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.
91. Paoletti LC & Blakemore RP (1986) Hydroxamate production by Aquaspirillum magnetotacticum. J Bacteriol 167: 73-76.
92. Philippe N & Wu LF (2010) An MCP-like protein interacts with the MamK cytoskeleton and is involved in magnetotaxis in Magnetospirillum magneticum AMB-1. J Mol Biol 400: 309-322.
93. Pósfai M, Buseck PR, Bazylinski DA & Frankel RB (1998) Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science 280: 880-883.
94. Pósfai M, Moskowitz BM, Arato 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: 444-455.
95. Pradel N, Santini CL, Bernadac A, Fukumori Y & Wu LF (2006) Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. P Natl Acad Sci USA 103: 17485-17489.
96. Prozorov T, Mallapragada SK, Narasimhan B et al. (2007a) Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv Funct Mater 17: 951-957.
97. Prozorov T, Palo P, Wang L, Nilsen-Hamilton M, Jones D, Orr D, Mallapragada SK, Narasimhan B, Canfield PC & Prozorov R (2007b) Cobalt ferrite nanocrystals: out-performing magnetotactic bacteria. ACS Nano 1: 228-233.
98. 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: 1075-1087.
99. Richter M, Kube M, Bazylinski DA, Lombardot T, Glöckner FO, Reinhardt R & Schüler D (2007) Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J Bacteriol 189: 4899-4910.
100. 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: e9151.
101. Romberg L & Levin PA (2003) Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu Rev Microbiol 57: 125-154.
102. Rudner DZ & Losick R (2010) Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2: a000307.
103. Rudner DZ, Pan Q & Losick RM (2002) Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. P Natl Acad Sci USA 99: 8701-8706.
104. Sakaguchi T, Burgess JG & Matsunaga T (1993) Magnetite formation by a sulfate-reducing bacterium. Nature 365: 47-49.
105. Savage DF, Afonso B, Chen AH & Silver PA (2010) Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327: 1258-1261.
106. 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: 6437-6446.
107. 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: 110-114.
108. 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: 377-386.
109. Schleifer KH, 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: 379-385.
110. Schmidt N, Mishra A, Lai GH & Wong GC (2010) Arginine-rich cell-penetrating peptides. FEBS Lett 584: 1806-1813.
111. 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: 5779-5790.
112. Schüler D & Baeuerlein E (1996) Iron-limited growth and kinetics of iron uptake in Magnetospirillum gryphiswaldense. Arch Microbiol 166: 301-307.
113. 4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180: 159-162.
114. Schültheiss D & Schüler D (2003) Development of a genetic system for Magnetospirillum gryphiswaldense. Arch Microbiol 179: 89-94.
115. Schumann D, Raub TD, Kopp RE et al. (2008) Gigantism in unique biogenic magnetite at the Paleocene-Eocene Thermal Maximum. P Natl Acad Sci USA 105: 17648-17653.
116. Shaevitz JW & Gitai Z (2010) The structure and function of bacterial actin homologs. Cold Spring Harb Perspect Biol 2: a000364.
117. Shapiro OH, Hatzenpichler R, Buckley DH, Zinder SH & Orphan VJ (2011) Multicellular photo-magnetotactic bacteria. Environ Microbiol Rep 3: 233-238.
118. 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.
119. Simmons SL, Bazylinski DA & Edwards KJ (2006) South-seeking magnetotactic bacteria in the Northern Hemisphere. Science 311: 371-374.
120. Simmons SL, Bazylinski DA & Edwards KJ (2007) Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ Microbiol 9: 2162-2174.
121. Smith MJ, Sheehan PE, Perry LL, O'Connor K, Csonka LN, Applegate BM & Whitman LJ (2006) Quantifying the magnetic advantage in magnetotaxis. Biophys J 91: 1098-1107.
122. 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.
123. 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: 158-162.
124. 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: 2275-2279.
125. 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: 5234-5247.
126. Tanaka M, Arakaki A & Matsunaga T (2010a) Identification and functional characterization of liposome tubulation protein from magnetotactic bacteria. Mol Microbiol 76: 480-488.
127. Tanaka M, Arakaki A, Staniland SS & Matsunaga T (2010b) Simultaneously discrete biomineralization of magnetite and tellurium nanocrystals in magnetotactic bacteria. Appl Environ Microbiol 76: 5526-5532.
128. Tanaka M, Mazuyama E, Arakaki A & Matsunaga T (2011) MMS6 protein regulates crystal morphology during nano-sized magnetite biomineralization in vivo. J Biol Chem 286: 6386-6392.
129. 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: 3805-3812.
130. Taoka A, Asada R, Wu L & Fukumori Y (2007) Polymerization of the actin-like protein MamK, which is associated with magnetosomes. J Bacteriol 189: 8737-8740.
131. Tocheva EI, Li Z & Jensen GJ (2010) Electron cryotomography. Cold Spring Harb Perspect Biol 2: a003442.
132. Uebe R, Voigt B, Schweder T, Albrecht D, Katzmann E, Lang C, Bottger L, Matzanke B & Schüler D (2010) Deletion of a fur-like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense. J Bacteriol 192: 4192-4204.
133. 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: 7176-7184.
134. Vainshtein M, Suzina N & Sorokin V (1997) A new type of magnet-sensitive inclusions in cells of photosynthetic purple bacteria. Syst Appl Microbiol 20: 182-186.
135. Vali H & Kirschvink J (1991) Observations of magnetosome organization, surface structure, and iron biomineralization of undescribed magnetic bacteria: evolutionary speculations. Iron Biominerals (Frankel RB & Blakemore RP, eds), pp. 97-116. Plenum Press, New York.
136. 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.
137. Weiner S (2008) Biomineralization: a structural perspective. J Struct Biol 163: 229-234.
138. Yamamoto D, Taoka A, Uchihashi T, Sasaki H, Watanabe H, Ando T & Fukumori Y (2010) Visualization and structural analysis of the bacterial magnetic organelle magnetosome using atomic force microscopy. P Natl Acad Sci USA 107: 9382-9387.
139. 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: 701-705.
140. Yijun H, Weijia Z, Wei J, Chengbo R & Ying L (2007) Disruption of a fur-like gene inhibits magnetosome formation in Magnetospirillum gryphiswaldense MSR-1. Biochem Mosc 72: 1247-1253.
141. Yoshino T, Maeda Y & Matsunag T (2010) Bioengineering of bacterial magnetic particles and their applications in biotechnology. Recent Pat Biotechnol 4: 214-225.
142. Zeytuni N, Ozyamak E, Ben-Harush K, Davidov G, Levin M, Gat Y, Moyal T, Brik A, Komeili A & Zarivach R (2011) Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly. P Natl Acad Sci USA 108: E480-E487.
143. Zurkiya O, Chan AW & Hu X (2008) MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn Reson Med 59: 1225-1231.