Skip to main content Accessibility help
×
Home

Formation of magnetic nanoparticle chains in bacterial systems

  • Damien Faivre (a1)

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.

Copyright

References

Hide All
1.Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Assmus, B., Schink, B., Nature 362, 834 (1993).
2.Croal, L.R., Gralnick, J.A., Malasarn, D., Newman, D.K., Annu. Rev. Genet. 38, 175 (2004).
3.Gralnick, J.A., Newman, D.K., Mol. Microbiol. 65, 1 (2007).
4.Frankel, R.B., Bazylinski, D.A., Rev. Mineral. Geochem. 54, 95 (2003).
5.Lin, W., Benzerara, K., Faivre, D., Pan, Y.X., Front. Microbiol. 5, (2014).
6.Bazylinski, D.A., Frankel, R.B., Rev. Mineral. Geochem. 54, 217 (2003).
7.Blakemore, R.P., Science 190, 377 (1975).
8.Schüler, D., FEMS Microbiol. Rev. 32, 654 (2008).
9.Cornejo, E., Abreu, N., Komeili, A., Curr. Opin. Cell Biol. 26, 132 (2014).
10.Lang, C., Schüler, D., Faivre, D., Macromol. Biosci. 7, 144 (2007).
11.Matsunaga, T., Suzuki, T., Tanaka, M., Arakaki, A., Trends Biotechnol. 25, 182 (2007).
12.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. 235250.
13.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).
14.Balkwill, D., Maratea, D., Blakemore, R.P., J. Bacteriol. 141, 1399 (1980).
15.Lefèvre, C.T., Bazylinski, D.A., Microbiol. Mol. Biol. Rev. 77, 497 (2013).
16.Mann, S., Frankel, R.B., Blakemore, R.P., Nature 310, 405 (1984).
17.Frankel, R.B., Papaefthymiou, G.C., Blakemore, R.P., O’Brien, W., Biochim. Biophys. Acta 763, 147 (1983).
18.Faivre, D., Böttger, L.H., Matzanke, B.F., Schüler, D., Angew. Chem. Int. Ed. 46, 8495 (2007).
19.Fdez-Gubieda, M.L., Muela, A., Alonso, J., García-Prieto, A., Olivi, L., Fernández-Pacheco, R., Barandiarán, J.M., ACS Nano 7, 3297 (2013).
20.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).
21.Mann, S., Sparks, N.H.C., Frankel, R.B., Bazylinski, D.A., Jannasch, H.W., Nature 343, 258 (1990).
22.Farina, M., Esquivel, D.M.S., Lins de Barros, H., Nature 343, 256 (1990).
23.Pósfai, M., Buseck, P.R., Bazylinski, D.A., Frankel, R.B., Science 280, 880 (1998).
24.Bazylinski, D.A., Heywood, B.R., Mann, S., Frankel, R.B., Nature 366, 218 (1993).
25.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).
26.Devouard, B., Posfai, M., Hua, X., Bazylinski, D.A., Frankel, R.B., Buseck, P.R., Am. Mineral. 83, 1387 (1998).
27.Körnig, A., Dong, J., Bennet, M., Widdrat, M., Andert, J., Müller, F.D., Schüler, D., Klumpp, S., Faivre, D., Nano Lett. 14, 4653 (2014).
28.Komeili, A., Li, Z., Newman, D.K., Jensen, G.J., Science 311, 242 (2006).
29.Scheffel, A., Gruska, M., Faivre, D., Linaroudis, A., Plitzko, J.M., Schüler, D., Nature 440, 110 (2006).
30.Faivre, D., Schüler, D., Chem. Rev. 108, 4875 (2008).
31.Gorby, Y.A., Beveridge, T.J., Blakemore, R., J. Bacteriol. 170, 834 (1988).
32.Grünberg, K., Müller, E.-C., Otto, A., Reszka, R., Linder, D., Kube, M., Reinhardt, R., Schüler, D., Appl. Environ. Microbiol. 70, 1040 (2004).
33.Matsunaga, T., Nemoto, M., Arakaki, A., Tanaka, M., Proteomics 9, 3341 (2009).
34.Grünberg, K., Wawer, C., Tebo, B.M., Schüler, D., Appl. Environ. Microbiol. 67, 4573 (2001).
35.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).
36.Ullrich, S., Kube, M., Schübbe, S., Reinhardt, R., Schüler, D., J. Bacteriol. 187, 7176 (2005).
37.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).
38.Jogler, C., Schüler, D., Annu. Rev. Microbiol. 63, 501 (2009).
39.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).
40.Murat, D., Falahati, V., Bertinetti, L., Csencsits, R., Körnig, A., Downing, K.H., Faivre, D., Komeili, A., Mol. Microbiol. 85, 684 (2012).
41.Murat, D., Quinlan, A., Vali, H., Komeili, A., Proc. Natl. Acad. Sci. U.S.A. 107, 5593 (2010).
42.Lohße, A., Borg, S., Raschdorf, O., Kolinko, I., Tompa, E., Posfai, M., Faivre, D., Baumgartner, J., Schüler, D., J. Bacteriol. 196, 2658 (2014).
43.Lohße, A., Ullrich, S., Katzmann, E., Borg, S., Wanner, G., Richter, M., Voigt, B., Schweder, T., Schüler, D., PLoS One 6, e25561 (2011).
44.Tanaka, M., Mazuyama, E., Arakaki, A., Matsunaga, T., J. Biol. Chem. 286, 6386 (2011).
45.Scheffel, A., Gärdes, A., Grünberg, K., Wanner, G., Schüler, D., J. Bacteriol. 190, 377 (2008).
46.Komeili, A., Vali, H., Beveridge, T.J., Newman, D., Proc. Natl. Acad. Sci. U.S.A. 101, 3839 (2004).
47.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).
48.Frankel, R.B., Bazylinski, D.A., Johnson, M.S., Taylor, B.L., Biophys. J. 73, 994 (1997).
49.Frankel, R.B., Williams, T.J., Bazylinski, D.A., in Magnetoreception and Magnetosomes in Bacteria, Schüler, D., Ed. (Springer, Heidelberg, 2007), vol. 3, pp. 124.
50.Bazylinski, D.A., Frankel, R.B., Nat. Rev. Microbiol. 2, 217 (2004).
51.Mao, X.G., Egli, R., Petersen, N., Hanzlik, M., Liu, X.M., PLoS One 9, e102810 (2014).
52.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).
53.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).
54.Popp, F., Armitage, J.P., Schüler, D., Nat. Commun. 5, 5398 (2014).
55.Alphandéry, E., Faure, S., Raison, L., Duguet, E., Howse, P.A., Bazylinski, D.A., J. Phys. Chem. C 115, 18 (2011).
56.Hergt, R., Hiergeist, R., Zeisberger, M., Schüler, D., Heyen, U., Hilger, I., Kaiser, W.A., J. Magn. Magn. Mater. 293, 80 (2005).
57.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).
58.Lisy, M.R., Hartung, A., Lang, C., Schüler, D., Richter, W., Reichenbach, J.R., Kaiser, W.A., Hilger, I., Invest. Radiol. 42, 235 (2007).
59.Prozorov, T., Bazylinski, D.A., Mallapragada, S.K., Prozorov, R., Mater. Sci. Eng. R 74, 133 (2013).
60.Yuan, J., Xu, Y., Müller, A.H.E., Chem. Soc. Rev. 40, 640 (2011).
61.Wang, H., Yu, Y., Sun, Y., Chen, Q., Nano 6, 1 (2011).
62.Ahniyaz, A., Sakamoto, Y., Bergström, L., Proc. Natl. Acad. Sci. U.S.A. 104, 17570 (2007).
63.Singh, G., Chan, H., Baskin, A., Gelman, E., Repnin, N., Krat, P., Klajn, R., Science 345, 1149 (2014).
64.Baumgartner, J., Bertinetti, L., Widdrat, M., Hirt, A.M., Faivre, D., PLoS One 8, e57070 (2013).
65.Widdrat, M., Kumari, M., Tomps, E., Posfai, M., Hirt, A.M., Faivre, D., ChemPlusChem, 79, 12251233 (2014).
66.Matsuda, T., Endo, J., Osakabe, N., Tonomura, A., Arii, T., Nature 302, 411 (1983).
67.Kopp, R.E., Kirschvink, J.L., Earth Sci. Rev. 86, 42 (2008).
68.Dunlop, D.J., Özdemir, O., Rock Magnetism: Fundamentals and Frontiers, Cambridge Studies in Magnetism (Cambridge University Press, Cambridge, 1997), p. 596.
69.Fleet, M., Acta Crystallogr. B 37, 917 (1981).
70.Fleet, M.E., Acta Crystallogr. C 40, 1491 (1984).
71.Fischer, A., Schmitz, M., Aichmayer, B., Fratzl, P., Faivre, D., J. R. Soc. Interface 8, 1011 (2011).
72.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).
73.Faivre, D., Ukmar Godec, T., Angew. Chem. Int. Ed. (2015). (forthcoming).
74.Muxworthy, A.R., Williams, W., J. Geophys. Res. 111, B12S12 (2006).
75.Muxworthy, A.R., Williams, W., J. R. Soc. Interface 6, 1207 (2009).
76.Rioux, J.B., Philippe, N., Pereira, S., Pignol, D., Wu, L.F., Ginet, N., PLoS One 5, 12 (2010).
77.Draper, O., Byrne, M.E., Li, Z., Keyhani, S., Barrozo, J.C., Jensen, G., Komeili, A., Mol. Microbiol. 82, 342 (2011).
78.Arakaki, A., Webbs, J., Matsunaga, T., J. Biol. Chem. 278, 8745 (2003).
79.Nudelman, H., Zarivach, R., Front. Microbiol. 5, 9 (2014).
80.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).
81.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).
82.Alphandéry, E., Ding, Y., Ngo, A.T., Wang, Z.L., Wu, L.F., Pileni, M.P., ACS Nano 3, 1539 (2009).
83.Dunin-Borkowski, R.E., McCartney, M.R., Frankel, R.B., Bazylinski, D.A., Pósfai, M., Buseck, P.R., Science 282, 1868 (1998).
84.Pósfai, M., Moskowitz, B.M., Arato, B., Schüler, D., Flies, C., Bazylinski, D.A., Frankel, R.B., Earth Planet. Sci. Lett. 249, 444 (2006).
85.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).
86.Lefèvre, C.T., Pósfai, M., Abreu, F., Lins, U., Frankel, R.B., Bazylinski, D.A., Earth Planet. Sci. Lett. 312, 194 (2011).
87.Körnig, A., Winklhofer, M., Baumgartner, J., Gonzalez, T.P., Fratzl, P., Faivre, D., Adv. Funct. Mater. 24, 3926 (2014).
88.Philipse, A.P., Maas, D., Langmuir 18, 9977 (2002).
89.Kiani, B., Faivre, D., Klumpp, S., New J. Phys. (forthcoming).
90.Abreu, N., Mannoubi, S., Ozyamak, E., Pignol, D., Ginet, N., Kimeili, A., J. Bacteriol. 196, 3111 (2014).
91.Ozyamak, E., Kollman, J., Agard, D.A., Komeili, A., J. Biol. Chem. 288, 4265 (2013).
92.Ozyamak, E., Kollman, J.M., Komeili, A., Biochemistry 52, 6928 (2013).
93.Carillo, M.A., Bennet, M., Faivre, D., J. Phys. Chem. B 117, 14642 (2013).
94.Taoka, A., Asada, R., Wu, L.F., Fukumori, Y., J. Bacteriol. 189, 8737 (2007).
95.Pradel, N., Santini, C.-L., Bernadac, A., Fukumori, Y., Wu, L.-F., Proc. Natl. Acad. Sci. U.S.A. 103, 17485 (2006).
96.Scheffel, A., Schüler, D., J. Bacteriol. 189, 6437 (2007).
97.Sonkaria, S., Fuentes, G., Verma, C., Narang, R., Khare, V., Fischer, A., Faivre, D., PLoS One 7, e34189 (2012).
98.Katzmann, E., Scheffel, A., Gruska, M., Plitzko, J.M., Schüler, D., Mol. Microbiol. 77, 208 (2010).
99.Kalirai, S.S., Bazylinski, D.A., Hitchcock, A.P., PLoS One 8, e53368 (2013).
100.Klumpp, S., Faivre, D.,PLoS One 7, e33562 (2012).
101.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.
102.Carvallo, C., Hickey, S., Faivre, D., Menguy, N., Earth Planets Space 61, 143 (2009).
103.Faivre, D., Fischer, A., Garcia-Rubio, I., Mastrogiacomo, G., Gehring, A.U., Biophys J. 99, 1268 (2010).
104.Katzmann, E., Müller, F.D., Lang, C., Messerer, M., Winklhofer, M., Plitzko, J.M., Schüler, D., Mol. Microbiol. 82, 1316 (2011).
105.Lefèvre, C.T., Bennet, M., Klumpp, S., Faivre, D., 6, 2 (2015), doi: 10.1128/mBio.02286-14.
106.Körnig, A., Hartmann, M.A., Teichert, C., Fratzl, P., Faivre, D., J. Phys. D Appl. Phys. 47, 235403 (2014).
107.Kirschvink, J.L., Automedica 14, 257 (1992).
108.Alphandéry, E., Faure, S., Seksek, O., Guyot, F., Chebbi, I., ACS Nano 5, 6279 (2011).
109.Taherkhani, S., Mohammadi, M., Daoud, J., Martel, S., Tabrizian, M., ACS Nano 8, 5049 (2014).

Keywords

Related content

Powered by UNSILO

Formation of magnetic nanoparticle chains in bacterial systems

  • Damien Faivre (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.