Biomimetic magnetite mediated by magnetosome proteins vs. ALH84001 meteorite magnetite: Are both comparable?
- Adrián Barry-Sosa Departamento de Microbiología. Facultad de Ciencias. Universidad de Granada, Campus de Fuentenueva s/n 18071, Granada,
- Concepción Jiménez-López Departamento de Microbiología. Facultad de Ciencias. Universidad de Granada, Campus de Fuentenueva s/n 18071, Granada
Abstract
The suggestion in 1996 that the Martian meteorite ALH84001 could contain proof of possible biologic activity in the past have generated a huge controversy that last until today. One of the most discussed evidence is the presence of magnetite crystals that resemble those produced by a particular group of bacteria, the so called magnetotactic bacteria (MTB). These microorganisms are the only known example of biologically controlled biomineralization among the prokaryotes and exert an exquisite control over the biomineralization process of intracellular magnetite that result in crystals with very unique features that, so far, cannot be replicated by inorganic means. These unique features have been used to recognize the biological origin of natural terrestrial magnetites, but the problem arises when those same biogenecity criteria are applied to extraterrestrial magnetites. Most of the problems are caused by the fact that it is not clear whether or not some of those characteristics can be reproduced inorganically. Magnetosome protein mediated magnetite synthesis seems to be the best approach to obtain magnetosome-like magnetites, and such strategy may help clarify what is the specific biosignature of magnetotactic bacteria.Downloads
References
Acuña, M. H., Connerney, J. E. P., Ness, N. F., Lin, R. P., Mitchell, D., Carlson, C.W., Mcfadden, J., Anderson, K.A., Rème, H., Mazelle, C., Vignes, D., Wasilewski, P., Cloutier, P. (1999) Global Distribution ofCrustal Magnetization Discovered by the Mars Global Surveyor MAG/ER Experiment . Science 284, 790-793.
Amor, M., Busigny, V., Durand-Dubief, M., Tharaud, M., Onanguem, G., Gélabert, A., Alphandéry, E., Menguy, N., Benedetti, M. F., Chebbi, I. Guyot, F. (2015) Chemical signature of magnetotactic bacteria. Proceedings of the National Academy of Science 112 (6), 1699-1703.
Amemiya, Y., Arakaki, A., Staniland, S.S., 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.
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. Journal of Colloid and Interface Science 343, 65–70.
Arakaki, A., Yamagishi, A., Fukuyo, A., Tanaka, M., Matsunaga, T. (2014) Co-ordinated functions of Mms proteins define the surface structure of cubooctahedral magnetite crystals in magnetotactic bacteria. Molecular Microbiology 93 (3), 554–567.
Arató, B., Szányi, Z., Flies, C., Schüler, D., Frankel, R. B., Buseck, P. R, Pósfai, M. (2005) Crystal‐size and shape distributions of magnetite from uncultured magnetotactic bacteria as a potential biomarker. American Mineralogist 90, 1233–1241.
Barber, D. J., Scott, E. R. (2002) Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001. Proceedings of the National Academy of Science 99 (10), 6556–6561.
Barber-Zucker, S., Keren-Khadmy, N., Zarivach, R. (2016) From invagination to navigation: The story of magnetosome associated proteins in magnetotactic bacteria. Protein Science 25 (2), 338-351.
Bazylinski, D. A., Frankel, R. B., Konhauser, K. O. (2007) Modes of Biomineralization of Magnetite by Microbes. Geomicrobiology Journal 24 (6), 465-475.
Bird, S.M., Galloway, J.M., Rawlings, A.E., Bramble, J.P., Staniland, S.S. (2015) Taking a hard line with biotemplating: cobalt doped magnetite magnetic nanoparticle arrays. Nanoscale 7, 7340–7351.
Brearley, A. J. (2003) Magnetite in ALH 84001: An origin by shock-induced thermal decomposition of iron carbonate. Meteoritics & Planetary Science 38 (6), 849–870.
Carter, J., Loizeau, D., Mangold, N., Poulet, F., Bibring, J.P. (2015) Widespread surface weathering on early Mars: A case for a warmer and wetter climate. Icarus 248, 373–382.
Devouard, B., Pósfai, M., Hua, X., Bazylinski, D. A., Frankel, R. B., Buseck, P. R. (1998) Magnetite from magnetotactic bacteria: Size distributions and twinning. American Mineralogist 83, 1387–1398.
Ding, Y., Li, J., Liu, J., Yang, J., Jiang, W., Tian, J., Li, Y., Pan, Y., Li, J. (2010) Deletion of the ftsZ-Like Gene Results in the Production of Superparamagnetic Magnetite Magnetosomes in Magnetospirillum gryphiswaldense. Journal of Bacteriology 192 (4), 1097–1105.
Draper, O., Byrne, M.E., Li, Z., Keyhani, S., Barrozo, J. C. Jensen, G. Komeili, A. (2011) MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Molecular Microbiology 82 (2), 342–354.
Frankel, R. B., And Blakemore, R. P. (1980) Navigational compass in magnetic bacteria. Journal of Magnetic Materials 15, 1562–1564.
Freissinet, C., Glavin, D. P., Mahaffy, P. R., Miller, K. E., Eigenbrode1, J. L., Summons, R. E., Brunner, A. E., Buch, A., Szopa, C., Archer Jr., P. D., Franz, H. B., Atreya, S. K., Brinckerhoff, W. B., Cabane, M., Coll, P., Conrad, P. G., Des Marais, D. J., Dworkin, J. P., Fairén, A. G., François, P., Grotzinger J. P., Kashyap, S., Kate, I. L., Leshin, L. A., Malespin, C. A., Martin, M. G., Martin-Torres, F. J., Mcadam, A. C., Ming, D. W., Navarro-González, R., Pavlov, A. A., Prats, B. D., Squyres, S. W., Steele, A., Stern, J. C., Sumner, D. Y., Sutter, B., Zorzano, M.-P., The Msl Science Team (2015) Organic molecules in the Sheepbed Mudstone, Gale Crater, Mars. Journal of Geophysical Research: Planets 120, 495–514.
Friedmann, E.I., Wierzchos, J., Ascaso, C., Winklhofer, M. (2001) Chains of magnetite crystals in the meteorite ALH84001: Evidence of biological origin. Proceeding of the National Academy of Science 98 (5), 2176–2181.
Galloway, J.M., Arakaki, A., Masuda, F., Tanaka, T., Matsunaga, T. Staniland, S.S. (2011) Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro. Journal of Materials Chemistry 21, 15244-15254.
Golden, D., Ming, D. W., Schwandt, C. S., Jr., H. V., Socki, R. A., Morris, R. V., Brearley, A.J., Lofgren, G. E., Mckay, G. A. (2001) A simple inorganic process for formation of carbonates, magnetite, and sulfides in Martian meteorite ALH84001. American Mineralogist 86, 370–375.
Golden, D., Ming, D., Morris, R., Brearley, A., Jr., H. L., Treiman, A., Lauer H.V. Jr., Treiman, A.H.; Zolensky, M.E.; Schwandt, C.S.; Lofgren, G.E., Mckay, G.A. (2004) Evidence for exclusively inorganic formation of magnetite in Martian meteorite ALH84001. American Mineralogist 89, 681–695.
Golden, D. C., Ming, D.W., Lauer, Jr. H.V., Morris, R.V., Treiman, A.H., Mckay G.A. (2006) Formation of “chemically pure” magnetite from Mg–Fe–carbonates: implications for the exclusively inorganic origin of magnetite and sulfides in Martian meteorite ALH84001. Lunar and Planetary. Sciences. XXXVII. Lunar Planet. Inst., Houston, nº 1199.
Gould, J. L., Kirschvink, J. L., Deffeyes, K. S. (1978) Bees Have Magnetic Remanence. Science 201 (4360), 1026-1028.
Grotzinger, J. P., Sumner, D. Y., Kah, L. C., Stack, K., Gupta, S., Edgar, L., Rubin, D., Lewis, K., Schieber, J., Mangold, N., Milliken, R., Conrad, P. G., Desmarais, D., Farmer J.,Siebach, Kcalef Iii, F., Hurowitz, J., Mclennan, S. M., Ming, D., Vaniman, D., Crisp, J., Vasavada A., Edgett, K. S., Malin, M., Blake, D., Gellert, R., Mahaffy, P., Wiens, R. C., Maurice, S., Grant, J. A., Wilson, S., Anderson, R. C., Beegle, L., Arvidson, R., Hallet, B.,Sletten, R. S., Rice, M., Bell Iii, J., Griffes, J., Ehlmann, B., Anderson, R. B., Bristow, T. F.,Dietrich, W. E., Dromart, G., Eigenbrode, J., Fraeman, A., Hardgrove, C., Herkenhoff, K., Jandura, L., Kocurek, G., Lee, S., Leshin, L. A., Leveille, R., Limonadi, D., Maki, J.,Mccloskey, S., Meyer, M., Minitti, M., Newsom, H., Oehler, D., Okon, A., Palucis, M., Parker, T., Rowland, S., Schmidt, M., Squyres, S., Steele, A., Stolper, E., Summons, R., Treiman, A., Williams, R., Yingst, A., Msl Science Team (2014) A Habitable Fluvio- Lacustrine Environment at Yellowknife Bay, Gale Crater, Mars. Science 343, (6169).
Grünberg, K., Müller, E.C., Otto, A., Reszka, R., Linder, D., Kube, M., Reinhardt, R., Schüler, D. (2004) Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Applied Environmental Microbiology 70, 1040–1050.
Ichinose N., Ozaki Y., Kashu S. (1992) In Superfine Particle Technology (Chap. 1) pp. 11–17.
Springer Verlag, London. Jiménez‐López, C., Romanek, C. S., Bazylinski, D. A. (2010) Magnetite as a prokaryotic biomarker: A review. Journal of Geophysical Research 115, G00G03.
Jiménez-López, C., Rodríguez-Navarro, C., Rodríguez-Navarro, A., Pérez-González, T., Bazylinski, D. A., Lauer, H. V., Romanek, Jr. C. S. (2012) Signatures in magnetites formed by (Ca,Mg,Fe)CO3 thermal decomposition: Terrestrial and extraterrestrial implications. Geochimica et Cosmochimica Acta 87, 69–80.
Jogler, C., Schüler, D. (2009) Genomics, genetics, and cell biology of magnetosome formation. Annual Review of Microbiology 63, 501–21.
Jones S.R., Wilson T.D., Brown M.E., Rahn-Lee L., Yu Y., Fredriksen L.L., Ozyamak E., Komeili A., Chang M.C.Y. (2015) Genetic and biochemical investigations of the role of MamP in redox control of iron biomineralization in Magnetospirillum magneticum. Proceedings of the National Academy of Science 112, 3904–3909.
Kashyap, S., Woehl, T., Valverde-Tercedor, C., Sánchez-Quesada, M., Jiménez-López, C., Prozorov, T. (2014) Visualization of Iron-Binding Micelles in Acidic Recombinant Biomineralization Protein, MamC. Journal of Nanomaterials Vol. 2014, Article ID 320124.
Katzmann, E., Scheffel, A., Gruska, M., Plitzko, J.M., Schüler, D. (2010) Loss of the actin-like protein MamK has pleiotropic effects on magnetosome formation and chain assembly in Magnetospirillum gryphiswaldense. Molecular Microbiology 77 (1), 208–224.
Kirschvink, J.L. (1982) Paleomagnetic evidence for fossil biogenic magnetite in western Crete. Earth and Planetary Science Letters 59, 388-392.
Kobayashi, A., Kirschvink, J.L., Nash, C.Z., Kopp, R.E., Sauer, D.A., Bertani, L.E., Voorhout, W.F., Taguchi, T. (2006) Experimental observation of magnetosome chain collapse in magnetotactic bacteria: Sedimentological, paleomagnetic, and evolutionary implications. Earth and Planetary Science Letters 245, 538–550.
Komeili, A., Li, Z., Newman, D. K., Jensen, G. J. (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311, 242-245.
Komeili, A. (2007) Molecular Mechanisms of Magnetosome Formation. Annual Reviews Biochemestry 76, 351–66.
Komeili, A. (2012) Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiology Reviews 36, 232–255.
Körnig, A., Winklhofer, M., Baumgartner, J., González, T. P., Fratzl, P., Faivre, D. (2014) Magnetite Crystal Orientation in Magnetosome Chains. Advanced. Functional Materials 24, 3926–3932.
Kopp, R.E., Nash, C.Z., Kobayashi, A., Weiss, B. P., Bazylinski, D.A., Kirschvink, J.L. (2006) Ferromagnetic resonance spectroscopy for assessment of magnetic anisotropy and magnetostatic interactions: A case study of mutant magnetotactic bacteria, Journal of Geophysical Research 111, B12S25.
Krasnopolsky, V.A. (2011) Atmospheric chemistry on Venus, Earth, and Mars: Main features and comparison. Planetary and Space Science 59, 952–964.
Lang, C., Schüler, D., Faivre, D. (2007) Synthesis of Magnetite Nanoparticles for Bio- and Nanotechnology: Genetic Engineering and Biomimetics of Bacterial Magnetosomes. Macromolecular Biosciences 7, 144–151.
Lang, C., Schüler, D. (2008) Expression of Green Fluorescent Protein Fused to Magnetosome Proteins in Microaerophilic Magnetotactic Bacteria. Applied and Environmental Microbiology 74 (15), 4944–4953.
Leshin, L. A., Mahaffy, P. R., Webster, C. R., Cabane, M., Coll, P., Conrad, P. G., Archer Jr., P. D., Atreya, S. K., Brunner, A. E., Buch, J.A., Eigenbrode, L., Flesch, G. J., Franz, H. B., Freissinet, C., Glavin, D. P., Mcadam, A. C., Miller, K. E., Ming, D. W., Morris, R. V., Navarro-González, R.,. Niles, P. B, Owen, T., Pepin, R. O., Squyres, S., Steele, A., Stern, J. C., Summons, R. E., Sumner, D. Y., Sutter, B., Szopa, C., Teinturier, S., Trainer, M. G., Wray, J. J., Grotzinger, J. P., Msl Science Team (2013) Volatile, Isotope, and Organic Analysis of Martian Fines with the Mars Curiosity Rover. Science 341, (6153). LIU, Y., CHEN, Q., (2008) Synthesis of magnetosome chain-like structures. Nanotechnology 19, 475603 (6pp).
Lohbe, A.,Borg, S.,Raschdorf, O., Kolinko, I., Tompa, É.,Pósfai, M., Faivre, D.,Baumgartner, J.,Schüler, D. (2014) Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense. Journal of Bacteriology 196 (14), 2658–2669.
Matsunaga, T., Suzuki, T., Tanaka, M., Arakaki, A. (2007) Molecular analysis of magnetotactic bacteria and development of functional bacterial magnetic particles for nano-biotechnology. TRENDS in Biotechnology 25 (4), 182-188.
Mckay, D. S., Gibson Jr., E. K., Thomas-Keprta, K. L., Vali, H., Romanek, C. S., Clemett, S. J., Simon J.,Chillier, X. D. F., Maechling, C. R., Zare, R.N. (1996) Search for Past Life on Mars: Possible Relic Biogenic Activity in Martian Meteorite ALH84001. Science 273, 924-930.
Müller, F.D., Raschdorf, O., Nudelman, H., Messerer, M., Katzmann, E., Plitzko, J.M., Zarivach, R., Schüler, D. (2014) The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation. Journal of Bacteriology 196 (3), 650–659.
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. Proceedings of the National Academy of Sciences 107, 5593–5598.
Murat, D., Falahati, V., Bertinetti, L., Csencsits, R., Körnig, A., Downing, K., Faivre, D., Komeili, A. (2012) The magnetosome membrane protein, MmsF, is a major regulator of magnetite biomineralization in Magnetospirillum magneticum AMB-1. Molecular Microbiology 85(4), 684–699.
Nesson, M.H., Lowenstam, H.A. (1985) Biomineralization processes of the radula teeth of chitons, in Magnetite biomineralization and magnetoreception in Organisms, edited by Kirschvink, J. L., Jones, D.S., MacFadden, B.J., Plenum Press, New York.
Nudelman, H., Zarivach, R. (2014) Structure prediction of magnetosome associated proteins. Frontiers in Microbiology 5, 9.
Paasche, Ø., Løvlie, R., Dahl, S. O., Bakke, J., Nesje, A. (2004) Bacterial magnetite in lake sediments: late glacial to Holocene climate and sedimentary changes in northern Norway. Earth and Planetary Science Letters 223, 319– 333.
Pérez-González, T., Valverde-Tercedor, C., Jiménez-López, C. (2010a). Biomineralización bacteriana de magnetita y aplicaciones. Seminario SEM 07, 58-64.
Pérez-González, T., Jiménez-López, C., Neal, A.L., Rull-Pérez, F., Rodríguez- Navarro, A., Fernández-Vivas, A., Iañez-Pareja, E. (2010b) Magnetite biomineralization induced by Shewanella oneidensis. Geochimica et Cosmochimica Acta 74, 967–979.
Perry, A., Bauer, G. B., Dizon, A.E. (1985) Magnetoreception and biomineralization of magnetite inamphibians and reptiles, in Magnetite biomineralization and magnetoreception in organisms,edited by Kirschvink, J. L., Jones, D.S., MacFadden, B.J., Plenum Press, New York.
Presti, D. E. (1985) Avian navigation, geomagnetic field sensitivity, andbiogenic magnetite, in Magnetite biomineralization and magnetoreception in organisms,edited by Kirschvink, J. L., Jones, D.S., MacFadden, B.J., Plenum Press, New York.
Prozorov, R., Prozorov, T., Mallapragada, S.K., Narasimhan, B., Williams, T.J., Bazylinski, D.A. (2007) Magnetic irreversibility and the Verwey transition in nanocrystalline bacterial magnetite. Physical Review B 76, 054406.
Prozorov, T., Mallapragada, S.K., Narasimhan, B., Wang, L., Palo, P., Nilsen-Hamilton, M., Williams, T.J., Bazylinski, D.A., Prozorov, R., Canfield, P.C. (2007) Protein-Mediated Synthesis of Uniform Superparamagnetic Magnetite Nanocrystals Advanced Functional Materials 17, 951–957.
Prozorov, T., Pérez-González, T., Valverde-Tercedor, C., Jiménez-López, C., Yebra-Rodríguez, A., Körnig, A., Faivre, D., Mallapragada, S.K., Howse, P.A., Bazylinski, D.A., Prozorov, R. (2014) Manganese incorporation into the magnetosome magnetite: magnetic signature of doping. European Journal of Mineralogy 26, 457–47.
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. Molecular Microbiology 80 (4), 1075–1087.
Raschdorf, O., Müller, F.D., Pósfai, M., Plitzko, J.M., Schüler, D. (2013) The magnetosome proteins MamX, MamZ and MamH are involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. Molecular Microbiology 89 (5), 872–886.
Rawlings, A.E., Bramble, J.P., Walker, R., Bain, J., Galloway, J. M., Staniland, S.S. (2014) Self-assembled MmsF proteinosomes control magnetitenanoparticle formation in vitro. Proceedings of the National Academy of Science 111 (45), 16094–16099.
Rawlings, A.E., Bramble, J.P., Hounslow A.M., Williamson M.P., Monnington A.E., Cooke D.J., Staniland S.S. (2016) Ferrous iron binding key to Mms6 magnetite biomineralisation: A mechanistic study to understand magnetite formation using pH titration and NMR spectroscopy. Chemistry - A European Journal 22(23), 7885–94.
Scheffel, A., Gruska, M., Faivre, D., Linaroudis, A., Plitzko, J. M., Schüler, D. (2006) An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440, 110-114.
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. Journal of Bacteriology 189 (17), 6437– 6446.
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. Journal of Bacteriology 190 (1), 377–386.
Siponen M.I., Adryanczyk, G., Ginet, N., Arnoux, P. Pignol, D. (2012) Magnetochrome: a c-type cytochrome domain specific to magnetotatic bacteria. Biochemical Society Transactions 40, 1319–1323.
Siponen, M.I., Legrand, P., Widdrat, M., Jones, S.R., Zhang, W.J., Chang, M.C.Y, Faivre, D., Arnoux, P., Pignol, D. (2013) Structural insight into magnetochrome-mediated magnetite biomineralization. Nature 502, 681- 684.
Snowball, I., Zillén, L., Sandgren, P. (2002) Bacterial magnetite in Swedish varved lake sediments: a potential bio-marker of environmental change. Quaternary International 88, 13–19.
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.
Tanaka, M., Mazuyama, E., Arakaki, A., Matsunaga, T. (2011) Mms6 Protein Regulates Crystal Morphology during Nano-sized Magnetite Biomineralization in Vivo. The Journal of Biological Chemistry 286 (8), 6386–6392.
Torres De Araujo, F. F., Pires, M. A., Frankel, R. B. , Bicudo, C. E. M. (1986) Magnetite and magnetotaxis in algae. Biophysical Journal 50, 375–378.
Thomas-Keprta, K., Bazylinski, D., Kirschvink, J. L., Clemett, S. J., Mckay, D. S., Wentworth, S. J., Vali, H., Gibson Jr, E. K .Romanek, C. S. (2000) Elongated prismatic magnetite crystals in ALH84001 carbonate globules: Potential Martian magnetofossils. Geochimica et Cosmochimica Acta 64 (23), 4049–4081.
Thomas-Keprta, K.L., Clemett, S.J., Bazylinski, D.A., Kirschvink, J.L., Mckay, D., Wentworth, S.J., Vali, H., Gibson, Jr., E. K., Mckay, M.F., Romanek., C.S. (2001) Truncated hexa- octahedral magnetite crystals in ALH84001: Presumptive biosignatures. Proceedings of the National Academy of Science 98 (5), 2164–2169.
Thomas-Keprta, K., Clemett, S., Mckay, D., Gibson, E., Wentworth, S. (2009) Origins of magnetite nanocrystals in Martian meteorite ALH84001. Geochimica et Cosmochimica Acta 73, 6631–6677.
Uebe, R., Junge, K., Henn, V., Poxleitner, G., Katzmann, E., Plitzko, J.M., Zarivach, R., Kasama, T., Wanner, G., Pósfai, M., Böttger, L., Matzanke, B., Schüler, D. (2011) The cation diffusion facilitator proteins MamB and MamM of Magnetospirillum gryphiswaldense have distinct and complex functions, and are involved in magnetite biomineralization and magnetosome membrane assembly. Molecular Microbiology 82, 818–835.
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. Journal of Bacteriology 187, 7176–7184.
Vali, H., Weiss, B., Li, Y.-L., Sears, S. K., Kim, S. S., Kirschvink, J. L., Zhang, C. L. (2004) Formation of tabular single-domain magnetite induced by Geobacter metallireducens GS-15. Proceedings of the National Academy of Science 101 (4), 16121-16126.
Valverde-Tercedor, C., Abadía-Molina, F., Martínez-Bueno, M., Pineda-Molina, E., Chen, L., Oestreicher, Z., Lower, B. H., Lower, S. K., Bazylinski, D. A. Jiménez-López, C. (2014) Subcellular localization of the magnetosome protein MamC in the marine magnetotactic bacterium Magnetococcus marinus strain MC-1 using immunoelectron microscopy. Archives of Microbiology 196, 481–488.
Valverde-Tercedor, C., Montalbán-López M., Pérez-González T., Sánchez-Quesada M.S., Prozorov T., Pineda- Molina E., Fernández-Vivas M.A., Rodríguez-Navarro, A.B., Trubitsyn, D., Bazylinski D.A., Jiménez-López, C. (2015) Size control of in vitro synthesized magnetite crystals by the MamC protein of Magnetococcus marinus strain MC-1. Applied Microbiology Biotechnology 99, 5109–5121.
Verwey, E. J. W. (1939) Electronic conduction of magnetite (Fe3O4) and its transition point at low temperatures. Nature 144, 327–328.
Vuong, T.K.O., Tran, D.L., Le, T.L., Pham, D.V., Pham, H.N., Ngo, T. H. L., Do, H. M., Nguyen, X.P. (2015) Synthesis of high-magnetization and monodisperse Fe3O4 nanoparticles via thermal decomposition. Materials Chemistry and Physics 163, 537-544.
Wang, L., Prozorov, T., Palo, P.E., Liu, X., Vaknin, D., Prozorov, R., Mallapragada, S., Nilsen-Hamilton, M. (2012) Self-assembly and biphasic iron-binding characteristics of Mms6, a bacterial protein that promotes the formation of superparamagnetic magnetite nanoparticles of uniform size and shape. Biomacromolecules 13, 98–105.
Weiss, B.P., Kim, S.S., Kirschvink, J.L., Kopp, R.E., Sankaran, M., Kobayashi, A., Komeili, A. (2004a) Magnetic tests for magnetosome chains in Martian meteorite ALH84001. Proceedings of the National Academy of Science 101 (22), 8281–8284.
Weiss, B. P., Kim, S. S., Kirschvink, J. L., Kopp, R. E., Sankaran, M., Kobayashi, A., Komeili, A. (2004b) Ferromagnetic resonance and low temperature magnetic tests for biogenic magnetite. Earth and Planetary Science Letters 224, 73–89.
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. Research in Microbiology 161, 701-705.
Yang, J., Li, S., Huang, X., Li J, Li, L., Pan, Y., Li, Y. (2013) MamX encoded by the mamXY operon is involved in control of magnetosome maturation in Magnetospirillum gryphiswaldense MSR-1. BMC Microbiology 13, 203.
Article download
Crossmark
