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Formation of magnetic nanoparticle chains in bacterial systems

Published online by Cambridge University Press:  03 June 2015

Damien Faivre
Damien Faivre*
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Germany; damien.faivre@mpikg.mpg.de
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Abstract

Several organisms possess a genetic program enabling them to form a mineral, a process termed biomineralization. The structure and composition of biominerals equip the biomineralizing organisms with functionalities that abiotic materials made of the same mineral do not necessarily possess. Even primary organisms such as bacteria are able to produce materials with properties superior to those of human-made equivalents. Magnetotactic bacteria represent a paradigm of such microorganisms. These organisms synthesize a hierarchical one-dimensional magnetic nanostructure based on the alignment of magnetosomes—organelles embedded in a vesicle dedicated to biomineralization and made of magnetic nanoparticles (magnetite (Fe3O4) or greigite (Fe3S4)). This article focuses on factors that play a role in the organization of these magnetosomes. The chains, which are based on aligned particles that have biologically controlled ultrastructure, size, morphology, organization, and orientation, serve as actuators and area means to align the bacteria with the Earth’s magnetic field lines when they swim in search of particular habitats in the aqueous environments they live in.

Keywords

magneticmagnetic propertiesbiologicalFeferromagnetic
Type
Research Article
Information
MRS Bulletin , Volume 40 , Issue 6: Biomineralization , June 2015 , pp. 509 - 515
Copyright
Copyright © Materials Research Society 2015 

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References

Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Assmus, B., Schink, B., Nature 362, 834 (1993).CrossRefGoogle Scholar
Croal, L.R., Gralnick, J.A., Malasarn, D., Newman, D.K., Annu. Rev. Genet. 38, 175 (2004).CrossRefGoogle Scholar
Gralnick, J.A., Newman, D.K., Mol. Microbiol. 65, 1 (2007).CrossRefGoogle Scholar
Frankel, R.B., Bazylinski, D.A., Rev. Mineral. Geochem. 54, 95 (2003).CrossRefGoogle Scholar
Lin, W., Benzerara, K., Faivre, D., Pan, Y.X., Front. Microbiol. 5, (2014).Google Scholar
Bazylinski, D.A., Frankel, R.B., Rev. Mineral. Geochem. 54, 217 (2003).CrossRefGoogle Scholar
Blakemore, R.P., Science 190, 377 (1975).CrossRefGoogle Scholar
Schüler, D., FEMS Microbiol. Rev. 32, 654 (2008).CrossRefGoogle Scholar
Cornejo, E., Abreu, N., Komeili, A., Curr. Opin. Cell Biol. 26, 132 (2014).CrossRefGoogle Scholar
Lang, C., Schüler, D., Faivre, D., Macromol. Biosci. 7, 144 (2007).CrossRefGoogle Scholar
Matsunaga, T., Suzuki, T., Tanaka, M., Arakaki, A., Trends Biotechnol. 25, 182 (2007).CrossRefGoogle Scholar
Carillo, M.A., Vach, P., Faivre, D., in Materials Design Inspired by Nature: Function through Inner Architecture, Fratzl, P., Dunlop, J.W.C., Weinkamer, R., Eds. (Royal Society of Chemistry, Cambridge, 2012), pp. 235–250.Google Scholar
McKay, D.S., Gibson, E.K. Jr., Thomas-Keprta, K.L., Vali, H., Romanek, C.S., Clemett, S.J., Chilier, X.D.F., Maechling, C.R., Science 273, 924 (1996).CrossRefGoogle Scholar
Balkwill, D., Maratea, D., Blakemore, R.P., J. Bacteriol. 141, 1399 (1980).CrossRefGoogle Scholar
Lefèvre, C.T., Bazylinski, D.A., Microbiol. Mol. Biol. Rev. 77, 497 (2013).CrossRefGoogle Scholar
Mann, S., Frankel, R.B., Blakemore, R.P., Nature 310, 405 (1984).CrossRefGoogle Scholar
Frankel, R.B., Papaefthymiou, G.C., Blakemore, R.P., O’Brien, W., Biochim. Biophys. Acta 763, 147 (1983).CrossRefGoogle Scholar
Faivre, D., Böttger, L.H., Matzanke, B.F., Schüler, D., Angew. Chem. Int. Ed. 46, 8495 (2007).CrossRefGoogle Scholar
Fdez-Gubieda, M.L., Muela, A., Alonso, J., García-Prieto, A., Olivi, L., Fernández-Pacheco, R., Barandiarán, J.M., ACS Nano 7, 3297 (2013).CrossRefGoogle Scholar
Baumgartner, J., Morin, G., Menguy, N., Perez Gonzalez, T., Widdrat, M., Cosmidis, J., Faivre, D., Proc. Natl. Acad. Sci. U.S.A. 110, 14883 (2013).CrossRefGoogle Scholar
Mann, S., Sparks, N.H.C., Frankel, R.B., Bazylinski, D.A., Jannasch, H.W., Nature 343, 258 (1990).CrossRefGoogle Scholar
Farina, M., Esquivel, D.M.S., Lins de Barros, H., Nature 343, 256 (1990).CrossRefGoogle Scholar
Pósfai, M., Buseck, P.R., Bazylinski, D.A., Frankel, R.B., Science 280, 880 (1998).CrossRefGoogle Scholar
Bazylinski, D.A., Heywood, B.R., Mann, S., Frankel, R.B., Nature 366, 218 (1993).CrossRefGoogle Scholar
Lefèvre, C.T., Menguy, N., Abreu, F., Lins, U., Pósfai, M., Prozorov, T., Pignol, D., Frankel, R.B., Bazylinski, D.A., Science 334, 1720 (2011).CrossRefGoogle Scholar
Devouard, B., Posfai, M., Hua, X., Bazylinski, D.A., Frankel, R.B., Buseck, P.R., Am. Mineral. 83, 1387 (1998).CrossRefGoogle Scholar
Körnig, A., Dong, J., Bennet, M., Widdrat, M., Andert, J., Müller, F.D., Schüler, D., Klumpp, S., Faivre, D., Nano Lett. 14, 4653 (2014).CrossRefGoogle Scholar
Komeili, A., Li, Z., Newman, D.K., Jensen, G.J., Science 311, 242 (2006).CrossRefGoogle Scholar
Scheffel, A., Gruska, M., Faivre, D., Linaroudis, A., Plitzko, J.M., Schüler, D., Nature 440, 110 (2006).CrossRefGoogle Scholar
Faivre, D., Schüler, D., Chem. Rev. 108, 4875 (2008).CrossRefGoogle Scholar
Gorby, Y.A., Beveridge, T.J., Blakemore, R., J. Bacteriol. 170, 834 (1988).CrossRefGoogle Scholar
Grünberg, K., Müller, E.-C., Otto, A., Reszka, R., Linder, D., Kube, M., Reinhardt, R., Schüler, D., Appl. Environ. Microbiol. 70, 1040 (2004).CrossRefGoogle Scholar
Matsunaga, T., Nemoto, M., Arakaki, A., Tanaka, M., Proteomics 9, 3341 (2009).CrossRefGoogle Scholar
Grünberg, K., Wawer, C., Tebo, B.M., Schüler, D., Appl. Environ. Microbiol. 67, 4573 (2001).CrossRefGoogle Scholar
Schübbe, S., Kube, M., Scheffel, A., Wawer, C., Heyen, U., Meyerdierks, A., Madkour, M., Mayer, F., Reinhardt, R., Schüler, D., J. Bacteriol. 185, 5779 (2003).CrossRefGoogle Scholar
Ullrich, S., Kube, M., Schübbe, S., Reinhardt, R., Schüler, D., J. Bacteriol. 187, 7176 (2005).CrossRefGoogle Scholar
Jogler, C., Wanner, G., Kolinko, S., Niebler, M., Amann, R., Petersen, N., Kube, M., Reinhardt, R., Schüler, D., Proc. Natl. Acad. Sci. U.S.A. 108, 1134 (2011).CrossRefGoogle Scholar
Jogler, C., Schüler, D., Annu. Rev. Microbiol. 63, 501 (2009).CrossRefGoogle Scholar
Abreu, F., Cantao, M.E., Nicolas, M.F., Barcellos, F.G., Morillo, V., Almeida, L.G.P., do Nascimento, F.F., Lefevre, C.T., Bazylinski, D.A., de Vasconcelos, A.T.R., Lins, U., ISME J. 5, 1634 (2011).CrossRefGoogle Scholar
Murat, D., Falahati, V., Bertinetti, L., Csencsits, R., Körnig, A., Downing, K.H., Faivre, D., Komeili, A., Mol. Microbiol. 85, 684 (2012).CrossRefGoogle Scholar
Murat, D., Quinlan, A., Vali, H., Komeili, A., Proc. Natl. Acad. Sci. U.S.A. 107, 5593 (2010).CrossRefGoogle Scholar
Lohße, A., Borg, S., Raschdorf, O., Kolinko, I., Tompa, E., Posfai, M., Faivre, D., Baumgartner, J., Schüler, D., J. Bacteriol. 196, 2658 (2014).CrossRefGoogle Scholar
Lohße, A., Ullrich, S., Katzmann, E., Borg, S., Wanner, G., Richter, M., Voigt, B., Schweder, T., Schüler, D., PLoS One 6, e25561 (2011).CrossRefGoogle Scholar
Tanaka, M., Mazuyama, E., Arakaki, A., Matsunaga, T., J. Biol. Chem. 286, 6386 (2011).CrossRefGoogle Scholar
Scheffel, A., Gärdes, A., Grünberg, K., Wanner, G., Schüler, D., J. Bacteriol. 190, 377 (2008).CrossRefGoogle Scholar
Komeili, A., Vali, H., Beveridge, T.J., Newman, D., Proc. Natl. Acad. Sci. U.S.A. 101, 3839 (2004).CrossRefGoogle Scholar
Kolinko, I., Lohsze, A., Borg, S., Raschdorf, O., Jogler, C., Tu, Q., Posfai, M., Tompa, E., Plitzko, J.M., Brachmann, A., Wanner, G., Muller, R., Zhang, Y., Schuler, D., Nat. Nanotechnol. 9, 193 (2014).CrossRefGoogle Scholar
Frankel, R.B., Bazylinski, D.A., Johnson, M.S., Taylor, B.L., Biophys. J. 73, 994 (1997).CrossRefGoogle Scholar
Frankel, R.B., Williams, T.J., Bazylinski, D.A., in Magnetoreception and Magnetosomes in Bacteria, Schüler, D., Ed. (Springer, Heidelberg, 2007), vol. 3, pp. 1–24.Google Scholar
Bazylinski, D.A., Frankel, R.B., Nat. Rev. Microbiol. 2, 217 (2004).CrossRefGoogle Scholar
Mao, X.G., Egli, R., Petersen, N., Hanzlik, M., Liu, X.M., PLoS One 9, e102810 (2014).CrossRefGoogle Scholar
Lefèvre, C.T., Bennet, M., Landau, L., Vach, P., Pignol, D., Bazylinski, D.A., Frankel, R.B., Klumpp, S., Faivre, D., Biophys. J. 107, 527 (2014).CrossRefGoogle Scholar
Bennet, M., McCarthy, A., Fix, D., Edwards, M.R., Repp, F., Vach, P., Dunlop, J.W.C., Sitti, M., Buller, G.S., Klumpp, S., Faivre, D., PLoS One 9, e101150 (2014).CrossRefGoogle Scholar
Popp, F., Armitage, J.P., Schüler, D., Nat. Commun. 5, 5398 (2014).CrossRefGoogle Scholar
Alphandéry, E., Faure, S., Raison, L., Duguet, E., Howse, P.A., Bazylinski, D.A., J. Phys. Chem. C 115, 18 (2011).CrossRefGoogle Scholar
Hergt, R., Hiergeist, R., Zeisberger, M., Schüler, D., Heyen, U., Hilger, I., Kaiser, W.A., J. Magn. Magn. Mater. 293, 80 (2005).CrossRefGoogle Scholar
Hartung, A., Lisy, M.R., Herrmann, K.-H., Hilger, I., Schüler, D., Lang, C., Bellmann, M.E., Kaiser, W.A., Reichenbach, R., J. Magn. Magn. Mater. 311, 454 (2007).CrossRefGoogle Scholar
Lisy, M.R., Hartung, A., Lang, C., Schüler, D., Richter, W., Reichenbach, J.R., Kaiser, W.A., Hilger, I., Invest. Radiol. 42, 235 (2007).CrossRefGoogle Scholar
Prozorov, T., Bazylinski, D.A., Mallapragada, S.K., Prozorov, R., Mater. Sci. Eng. R 74, 133 (2013).CrossRefGoogle Scholar
Yuan, J., Xu, Y., Müller, A.H.E., Chem. Soc. Rev. 40, 640 (2011).CrossRefGoogle Scholar
Wang, H., Yu, Y., Sun, Y., Chen, Q., Nano 6, 1 (2011).CrossRefGoogle ScholarPubMed
Ahniyaz, A., Sakamoto, Y., Bergström, L., Proc. Natl. Acad. Sci. U.S.A. 104, 17570 (2007).CrossRefGoogle Scholar
Singh, G., Chan, H., Baskin, A., Gelman, E., Repnin, N., Krat, P., Klajn, R., Science 345, 1149 (2014).CrossRefGoogle Scholar
Baumgartner, J., Bertinetti, L., Widdrat, M., Hirt, A.M., Faivre, D., PLoS One 8, e57070 (2013).CrossRefGoogle Scholar
Widdrat, M., Kumari, M., Tomps, E., Posfai, M., Hirt, A.M., Faivre, D., ChemPlusChem, 79, 1225–1233 (2014).CrossRefGoogle Scholar
Matsuda, T., Endo, J., Osakabe, N., Tonomura, A., Arii, T., Nature 302, 411 (1983).CrossRefGoogle Scholar
Kopp, R.E., Kirschvink, J.L., Earth Sci. Rev. 86, 42 (2008).CrossRefGoogle Scholar
Dunlop, D.J., Özdemir, O., Rock Magnetism: Fundamentals and Frontiers, Cambridge Studies in Magnetism (Cambridge University Press, Cambridge, 1997), p. 596.CrossRefGoogle Scholar
Fleet, M., Acta Crystallogr. B 37, 917 (1981).CrossRefGoogle Scholar
Fleet, M.E., Acta Crystallogr. C 40, 1491 (1984).CrossRefGoogle Scholar
Fischer, A., Schmitz, M., Aichmayer, B., Fratzl, P., Faivre, D., J. R. Soc. Interface 8, 1011 (2011).CrossRefGoogle Scholar
Thomas-Keprta, K.L., Bazylinski, D.A., Kirschvink, J.L., Clemett, S.J., McKay, D.S., Wentworth, S.J., Vali, H., Gibson, E.K. Jr., Romanek, C.S., Geochim. Cosmochim. Acta 64, 4049 (2000).CrossRefGoogle Scholar
Faivre, D., Ukmar Godec, T., Angew. Chem. Int. Ed. (2015). (forthcoming).Google Scholar
Muxworthy, A.R., Williams, W., J. Geophys. Res. 111, B12S12 (2006).Google Scholar
Muxworthy, A.R., Williams, W., J. R. Soc. Interface 6, 1207 (2009).CrossRefGoogle Scholar
Rioux, J.B., Philippe, N., Pereira, S., Pignol, D., Wu, L.F., Ginet, N., PLoS One 5, 12 (2010).CrossRefGoogle Scholar
Draper, O., Byrne, M.E., Li, Z., Keyhani, S., Barrozo, J.C., Jensen, G., Komeili, A., Mol. Microbiol. 82, 342 (2011).CrossRefGoogle Scholar
Arakaki, A., Webbs, J., Matsunaga, T., J. Biol. Chem. 278, 8745 (2003).CrossRefGoogle Scholar
Nudelman, H., Zarivach, R., Front. Microbiol. 5, 9 (2014).CrossRefGoogle Scholar
Zeytuni, N., Ozyamak, E., Ben-Harush, K., Davidov, G., Levin, M., Gat, Y., Moyal, T., Brik, A., Komeili, A., Zarivach, R., Proc. Natl. Acad. Sci. U.S.A. 108, E480 (2011).CrossRefGoogle Scholar
Siponen, M.I., Legrand, P., Widdrat, M., Jones, S.R., Zhang, W.-J., Chang, M.C.Y., Faivre, D., Arnoux, P., Pignol, D., Nature 502, 681 (2013).CrossRefGoogle Scholar
Alphandéry, E., Ding, Y., Ngo, A.T., Wang, Z.L., Wu, L.F., Pileni, M.P., ACS Nano 3, 1539 (2009).CrossRefGoogle Scholar
Dunin-Borkowski, R.E., McCartney, M.R., Frankel, R.B., Bazylinski, D.A., Pósfai, M., Buseck, P.R., Science 282, 1868 (1998).CrossRefGoogle Scholar
Pósfai, M., Moskowitz, B.M., Arato, B., Schüler, D., Flies, C., Bazylinski, D.A., Frankel, R.B., Earth Planet. Sci. Lett. 249, 444 (2006).CrossRefGoogle Scholar
Li, J.H., Pan, Y.X., Liu, Q.S., Kui, Y.Z., Menguy, N., Che, R.C., Qin, H.F., Lin, W., Wu, W.F., Petersen, N., Yang, X.A., Earth Planet. Sci. Lett. 293, 368 (2010).CrossRefGoogle Scholar
Lefèvre, C.T., Pósfai, M., Abreu, F., Lins, U., Frankel, R.B., Bazylinski, D.A., Earth Planet. Sci. Lett. 312, 194 (2011).CrossRefGoogle Scholar
Körnig, A., Winklhofer, M., Baumgartner, J., Gonzalez, T.P., Fratzl, P., Faivre, D., Adv. Funct. Mater. 24, 3926 (2014).CrossRefGoogle Scholar
Philipse, A.P., Maas, D., Langmuir 18, 9977 (2002).CrossRefGoogle Scholar
Kiani, B., Faivre, D., Klumpp, S., New J. Phys. (forthcoming).Google Scholar
Abreu, N., Mannoubi, S., Ozyamak, E., Pignol, D., Ginet, N., Kimeili, A., J. Bacteriol. 196, 3111 (2014).CrossRefGoogle Scholar
Ozyamak, E., Kollman, J., Agard, D.A., Komeili, A., J. Biol. Chem. 288, 4265 (2013).CrossRefGoogle Scholar
Ozyamak, E., Kollman, J.M., Komeili, A., Biochemistry 52, 6928 (2013).CrossRefGoogle Scholar
Carillo, M.A., Bennet, M., Faivre, D., J. Phys. Chem. B 117, 14642 (2013).CrossRefGoogle Scholar
Taoka, A., Asada, R., Wu, L.F., Fukumori, Y., J. Bacteriol. 189, 8737 (2007).CrossRefGoogle Scholar
Pradel, N., Santini, C.-L., Bernadac, A., Fukumori, Y., Wu, L.-F., Proc. Natl. Acad. Sci. U.S.A. 103, 17485 (2006).CrossRefGoogle Scholar
Scheffel, A., Schüler, D., J. Bacteriol. 189, 6437 (2007).CrossRefGoogle Scholar
Sonkaria, S., Fuentes, G., Verma, C., Narang, R., Khare, V., Fischer, A., Faivre, D., PLoS One 7, e34189 (2012).CrossRefGoogle Scholar
Katzmann, E., Scheffel, A., Gruska, M., Plitzko, J.M., Schüler, D., Mol. Microbiol. 77, 208 (2010).CrossRefGoogle Scholar
Kalirai, S.S., Bazylinski, D.A., Hitchcock, A.P., PLoS One 8, e53368 (2013).CrossRefGoogle Scholar
Klumpp, S., Faivre, D.,PLoS One 7, e33562 (2012).CrossRefGoogle Scholar
Bennet, M., Bertinetti, L., Neely, R.K., Schertel, A., Kornig, A., Flors, C., Muller, F.D., Schuler, D., Klumpp, S., Faivre, D., Faraday Discuss. (2014), doi: 10.1039/c4fd00240g.Google Scholar
Carvallo, C., Hickey, S., Faivre, D., Menguy, N., Earth Planets Space 61, 143 (2009).CrossRefGoogle Scholar
Faivre, D., Fischer, A., Garcia-Rubio, I., Mastrogiacomo, G., Gehring, A.U., Biophys J. 99, 1268 (2010).CrossRefGoogle Scholar
Katzmann, E., Müller, F.D., Lang, C., Messerer, M., Winklhofer, M., Plitzko, J.M., Schüler, D., Mol. Microbiol. 82, 1316 (2011).CrossRefGoogle Scholar
Lefèvre, C.T., Bennet, M., Klumpp, S., Faivre, D., 6, 2 (2015), doi: 10.1128/mBio.02286-14.CrossRefGoogle Scholar
Körnig, A., Hartmann, M.A., Teichert, C., Fratzl, P., Faivre, D., J. Phys. D Appl. Phys. 47, 235403 (2014).CrossRefGoogle Scholar
Kirschvink, J.L., Automedica 14, 257 (1992).Google Scholar
Alphandéry, E., Faure, S., Seksek, O., Guyot, F., Chebbi, I., ACS Nano 5, 6279 (2011).CrossRefGoogle Scholar
Taherkhani, S., Mohammadi, M., Daoud, J., Martel, S., Tabrizian, M., ACS Nano 8, 5049 (2014).CrossRefGoogle Scholar