Abstract
Magnetotactic bacteria swim along the magnetic field using a unique bacterial organelle termed the magnetosome. Magnetosomes are comprised of nano-sized crystals of magnetite or greigite enclosed within lipid bilayer membrane vesicles and specifically associated proteins. The integration of magnetosomes in motility allows magnetotactic bacteria to orient themselves to find a favorable microaerobic habitat. Most of the magnetosome-associated proteins are encoded in gene clusters within a “magnetosome island.” Additionally, these proteins are highly conserved and essential for the synthesis and maintenance of magnetosomes. In this chapter, we will briefly introduce general insight into magnetotactic bacteria, and then, we will present recent research progress on magnetosome structure and function.
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References
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(Pt 6):1318–1322. https://doi.org/10.1099/ijs.0.64857-0
Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2(3):217–230. https://doi.org/10.1038/nrmicro842
Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic magnetite production by a marine, magnetotactic bacterium. Nature 334:518–519
Bellini S (2009a) Further studies on “magnetosensitive bacteria”. Chin J Oceanol Limnol 27(1):6–12. https://doi.org/10.1007/s00343-009-0006-2
Bellini S (2009b) On a unique behavior of freshwater bacteria. Chin J Oceanol Limnol 27(1):3–5. https://doi.org/10.1007/s00343-009-0003-5
Bergeron JR, Hutto R, Ozyamak E, Hom N, Hansen J, Draper O, Byrne ME, Keyhani S, Komeili A, Kollman JM (2016) Structure of the magnetosome-associated actin-like MamK filament at subnanometer resolution. Protein Sci. https://doi.org/10.1002/pro.2979
Blakemore R (1975) Magnetotactic bacteria. Science 190(4212):377–379
Blakemore RP (1982) Magnetotactic bacteria. Annu Rev Microbiol 36:217–238. https://doi.org/10.1146/annurev.mi.36.100182.001245
Blakemore RP, Maratea D, Wolfe RS (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140(2):720–729
Bork P, Sander C, Valencia A (1992) An ATPase domain common to prokaryotic cell-cycle proteins, sugar kinases, actin, and Hsp70 heat-shock proteins. Proc Natl Acad Sci U S A 89(16):7290–7294. https://doi.org/10.1073/pnas.89.16.7290
Deng A, Lin W, Shi N, Wu J, Sun Z, Sun Q, Bai H, Pan Y, Wen T (2016) In vitro assembly of the bacterial actin protein MamK from ‘Candidatus Magnetobacterium casensis’ in the phylum Nitrospirae. Protein Cell 7(4):267–280. https://doi.org/10.1007/s13238-016-0253-x
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(4):534–552. https://doi.org/10.1111/j.1365-2958.2009.06771.x
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(2):342–354. https://doi.org/10.1111/j.1365-2958.2011.07815.x
Dufrêne YF (2008) Towards nanomicrobiology using atomic force microscopy. Nat Rev Microbiol 6(9):674–680. https://doi.org/10.1038/nrmicro1948
Engel A, Müller DJ (2000) Observing single biomolecules at work with the atomic force microscope. Nat Struct Biol 7(9):715–718. https://doi.org/10.1038/78929
Faivre D, Schüler D (2008) Magnetotactic bacteria and magnetosomes. Chem Rev 108(11):4875–4898. https://doi.org/10.1021/cr078258w
Flies CB, Peplies J, Schüler D (2005) Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol 71(5):2723–2731. https://doi.org/10.1128/Aem.71.5.2723-2731.2005
Frankel RB (2009) The discovery of magnetotactic/magnetosensitive bacteria. Chin J Oceanol Limnol 27(1):1–2. https://doi.org/10.1007/s00343-009-0001-7
Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73(2):994–1000
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(3):801–812. https://doi.org/10.1016/j.febstet.2006.01.003
Gorlenko VM, Dzyuba MV, Maleeva AN, Panteleeva AN, Kolganova TV, Kuznetsov BB (2011) Magnetospirillum aberrantis sp. nov., a new freshwater bacterium with magnetic inclusions. Microbiology 80(5):692–702. https://doi.org/10.1134/S0026261711050055
Jogler C, Lin W, Meyerdierks A, Kube M, Katzmann E, Flies C, Pan YX, Amann R, Reinhardt R, Schüler D (2009) Toward cloning of the magnetotactic metagenome: identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol 75(12):3972–3979. https://doi.org/10.1128/Aem.02701-08
Jones LJF, Carballido-López R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104(6):913–922. https://doi.org/10.1016/S0092-8674(01)00287-2
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(7):1709–1721. https://doi.org/10.1111/j.1462-2920.2011.02609.x
Kolinko S, Wanner G, Katzmann E, Kiemer F, Fuchs BM, Schüler D (2013) Clone libraries and single cell genome amplification reveal extended diversity of uncultivated magnetotactic bacteria from marine and freshwater environments. Environ Microbiol 15(5):1290–1301. https://doi.org/10.1111/1462-2920.12004
Komeili A (2012) Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiol Rev 36(1):232–255. https://doi.org/10.1111/j.1574-6976.2011.00315.x
Komeili A, Li Z, Newman DK, Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311(5758):242–245. https://doi.org/10.1126/science.1123231
Kruse T, Møller-Jensen J, Løbner-Olesen A, Gerdes K (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22(19):5283–5292. https://doi.org/10.1093/emboj/cdg504
Lefèvre CT, Bazylinski DA (2013) Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev: MMBR 77(3):497–526. https://doi.org/10.1128/MMBR.00021-13
Lefèvre CT, Wu LF (2013) Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol 21(10):534–543. https://doi.org/10.1016/j.tim.2013.07.005
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(7):1646–1657. https://doi.org/10.1111/j.1462-2920.2009.01887.x
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(11):3740–3743. https://doi.org/10.1128/Aem.03018-09
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(2):538–549. https://doi.org/10.1111/j.1462-2920.2010.02361.x
Lefèvre CT, Frankel RB, Pósfai M, Prozorov T, Bazylinski DA (2011b) Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ Microbiol 13(8):2342–2350. https://doi.org/10.1111/j.1462-2920.2011.02505.x
Lefèvre CT, Menguy N, Abreu F, Lins U, Pósfai M, Prozorov T, Pignol D, Frankel RB, Bazylinski DA (2011c) A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 334(6063):1720–1723. https://doi.org/10.1126/science.1212596
Lefèvre CT, Viloria N, Schmidt ML, Posfai M, Frankel RB, Bazylinski DA (2012) Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J 6(2):440–450. https://doi.org/10.1038/ismej.2011.97
Lefèvre CT, Trubitsyn D, Abreu F, Kolinko S, de Almeida LGP, de Vasconcelos ATR, Lins U, Schüler D, Ginet N, Pignol D, Bazylinski DA (2013) Monophyletic origin of magnetotaxis and the first magnetosomes. Environ Microbiol 15(8):2267–2274. https://doi.org/10.1111/1462-2920.12097
Li WB, Yu LJ, Zhou PP, Min Z (2007) Isolation of magnetotactic bacterium WM-1 from freshwater sediment and phylogenetic characterization. Arch Microbiol 188(1):97–102. https://doi.org/10.1007/s00203-007-0231-z
Lin W, Li JH, Pan YX (2012) Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl Environ Microbiol 78(3):668–675. https://doi.org/10.1128/Aem.06764-11
Lin W, Bazylinski DA, Xiao T, Wu LF, Pan Y (2013) Life with compass: diversity and biogeography of magnetotactic bacteria. Environ Microbiol 16(9):2646–2658. https://doi.org/10.1111/1462-2920.12313
Lin W, Deng AH, Wang Z, Li Y, Wen TY, Wu LF, Wu M, Pan YX (2014) Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae. ISME J 8(12):2463–2477. https://doi.org/10.1038/ismej.2014.94
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(10):e25561. https://doi.org/10.1371/journal.pone.0025561
Matsunaga T, Sakaguchi T, Tadokoro F (1991) Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol 35(5):651–655
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(3):157–166. https://doi.org/10.1093/dnares/dsi002
Meldrum FC, Mann S, Heywood BR, Frankel RB, Bazylinski DA (1993a) Electron microscopy study of magnetosomes in two cultured vibrioid magnetotactic bacteria. Proc R Soc Lond B Biol Sci 251(1332):237–242
Meldrum FC, Mann S, Heywood BR, Frankel RB, Bazylinski DA (1993b) Electron-microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium. Proc R Soc B-Biol Sci 251(1332):231–236. https://doi.org/10.1098/rspb.1993.0034
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 U S A 107(12):5593–5598. https://doi.org/10.1073/pnas.0914439107
Nguyen HV, Suzuki E, Oestreicher Z, Minamide H, Endoh H, Fukumori Y, Taoka A (2016) A protein-protein interaction in magnetosomes: TPR protein MamA interacts with an Mms6 protein. Biochem Biophys Rep 7:39–44. https://doi.org/10.1016/j.bbrep.2016.05.010
Okuda Y, Fukumori Y (2001) Expression and characterization of a magnetosome-associated protein, TPR-containing MAM22, in Escherichia coli. FEBS Lett 491(3):169–173. https://doi.org/10.1016/S0014-5793(01)02178-0
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(1):99–102. https://doi.org/10.1016/0378-1119(95)00008-9
Ozyamak E, Kollman J, Agard DA, Komeili A (2013) The bacterial actin MamK: in vitro assembly behavior and filament architecture. J Biol Chem 288(6):4265–4277. https://doi.org/10.1074/jbc.M112.417030
Pan WD, Xie CL, Lv J (2012) Screening for the interacting partners of the proteins MamK & MamJ by two-hybrid genomic DNA library of Magnetospirillum magneticum AMB-1. Curr Microbiol 64(6):515–523. https://doi.org/10.1007/s00284-012-0099-2
Petersen N, Weiss DG, Vali H (1989) Magnetic bacteria in lake sediments. Geomagnetism and palaeomagnetism, The NATO ASI Series, vol 261. Springer, Berlin, pp 231–241
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(3):309–322. https://doi.org/10.1016/j.jmb.2010.05.011
Revathy T, Jacob JJ, Jayasri MA, Suthindhiran K (2016) Isolation and characterization of Magnetospirillum from saline lagoon. World J Microbiol Biotechnol 32(7):109. https://doi.org/10.1007/s11274-016-2075-7
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(13):4899–4910. https://doi.org/10.1128/Jb.00119-07
Sakaguchi T, Burgess JG, Matsunaga T (1993) Magnetite formation by a sulfate-reducing bacterium. Nature 365(6441):47–49. https://doi.org/10.1038/365047a0
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(17):6437–6446. https://doi.org/10.1128/Jb.00421-07
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(7080):110–114. https://doi.org/10.1038/nature04382
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(4):379–385
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(19):5779–5790. https://doi.org/10.1128/Jb.185.19.5779-5790.2003
Schüler D (2008) Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiol Rev 32(4):654–672. https://doi.org/10.1111/j.1574-6976.2008.00116.x
Shaevitz JW, Gitai Z (2010) The structure and function of bacterial actin homologs. Cold Spring Harb Perspect Biol 2(9):a000364. https://doi.org/10.1101/cshperspect.a000364
Sonkaria S, Fuentes G, Verma C, Narang R, Khare V, Fischer A, Faivre D (2012) Insight into the assembly properties and functional organisation of the magnetotactic bacterial actin-like homolog, MamK. PLoS One 7(5):e34189. https://doi.org/10.1371/journal.pone.0034189
Taoka A, Asada R, Sasaki H, Anzawa K, Wu L, Fukumori Y (2006) Spatial localizations of Mam22 and Mam12 in the magnetosomes of Magnetospirillum magnetotacticum. J Bacteriol 188(11):3805–3812. https://doi.org/10.1128/JB.00020-06
Taoka A, Asada R, Wu L-F, Fukumori Y (2007) Polymerization of the actin-like protein MamK, which is associated with magnetosomes. J Bacteriol 189(23):8737–8740. https://doi.org/10.1128/JB.00899-07
Taoka A, Kondo J, Oestreicher Z, Fukumori Y (2014) Characterization of uncultured giant rod-shaped magnetotactic Gammaproteobacteria from a freshwater pond in Kanazawa, Japan. Microbiol-SGM 160:2226–2234. https://doi.org/10.1099/mic.0.078717-0
Thrash JC, Ahmadi S, Torok T, Coates JD (2010) Magnetospirillum bellicus sp. nov., a novel dissimilatory perchlorate-reducing Alphaproteobacterium isolated from a bioelectrical reactor. Appl Environ Microbiol 76(14):4730–4737. https://doi.org/10.1128/Aem.00015-10
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(21):7176–7184. https://doi.org/10.1128/Jb.187.21.7176-7184.2005
van den Ent F, Amos LA, Löwe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413(6851):39–44. https://doi.org/10.1038/35092500
van den Ent F, Møller-Jensen J, Amos LA, Gerdes K, Löwe J (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J 21(24):6935–6943. https://doi.org/10.1093/emboj/cdf672
Wang YZ, Lin W, Li JH, Zhang TW, Li Y, Tian JS, Gu LX, Heyden YV, Pan YX (2015) Characterizing and optimizing magnetosome production of Magnetospirillum sp XM-1 isolated from Xi’an City Moat, China. FEMS Microbiol Lett 362(21):fnv167. https://doi.org/10.1093/femsle/fnv167
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(6):1493–1505. https://doi.org/10.1111/j.1462-2920.2009.01877.x
Williams TJ, Lefèvre CT, Zhao WD, Beveridge TJ, Bazylinski DA (2012) Magnetospira thiophila gen. nov., sp. nov., a marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae (Alphaproteobacteria). Int J Syst Evol Microbiol 62:2443–2450. https://doi.org/10.1099/ijs.0.037697-0
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. Proc Natl Acad Sci U S A 107(20):9382–9387. https://doi.org/10.1073/pnas.1001870107
Zeytuni N, Zarivach R (2012) Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure 20(3):397–405. https://doi.org/10.1016/j.str.2012.01.006
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. Proc Natl Acad Sci U S A 108(33):E480–E487. https://doi.org/10.1073/pnas.1103367108
Zeytuni N, Baran D, Davidov G, Zarivach R (2012) Inter-phylum structural conservation of the magnetosome-associated TPR-containing protein, MamA. J Struct Biol 180(3):479–487. https://doi.org/10.1016/j.jsb.2012.08.001
Zeytuni N, Cronin S, Lefèvre CT, Arnoux P, Baran D, Shtein Z, Davidov G, Zarivach R (2015) MamA as a model protein for structure-based insight into the evolutionary origins of magnetotactic bacteria. PLoS One 10(6):e0130394. https://doi.org/10.1371/journal.pone.0130394
Zhang WY, Zhou K, Pan HM, Yue HD, Jiang M, Xiao T, Wu LF (2012) Two genera of magnetococci with bean-like morphology from intertidal sediments of the yellow sea, China. Appl Environ Microbiol 78(16):5606–5611. https://doi.org/10.1128/Aem.00081-12
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(2):405–413. https://doi.org/10.1111/j.1462-2920.2011.02590.x
Zhu KL, Pan HM, Li JH, Yu-Zhang K, Zhang SD, Zhang WY, Zhou K, Yue HD, Pan YX, Xiao TA, 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(4):276–283. https://doi.org/10.1016/j.resmic.2010.02.003
Zhu X, Ge X, Li N, Wu LF, Luo C, Ouyang Q, Tu Y, Chen G (2014) Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1. Integr Biol 6(7):706–713. https://doi.org/10.1039/c3ib40259b
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This work was supported by MEXT KAKENHI (24117007 and 23111508), JSPS KAKENHI (17H03791, 16 K07661, 25850051, and 22780063), the Human Frontier Science Program (RGP0035/2004-C104), and the Institute for Fermentation, Osaka (IFO).
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Taoka, A., Fukumori, Y. (2018). Structure and Function of Aligned Magnetic Crystals in Magnetotactic Bacteria. In: Matsunaga, T., Tanaka, T., Kisailus, D. (eds) Biological Magnetic Materials and Applications. Springer, Singapore. https://doi.org/10.1007/978-981-10-8069-2_1
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