Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Magnetosome biogenesis in magnetotactic bacteria

Nature Reviews Microbiology volume 14, pages 621–637 (2016)Cite this article

Subjects

Key Points

  • The orientation of magnetotactic bacteria is based on the presence of unique organelles, magnetosomes, which are intracellular, membrane-enclosed, nanometre-sized crystals of magnetic iron minerals.

  • In the past decade, substantial advances have been made in our understanding of magnetosome biogenesis using two genetically tractable Magnetospirillum species.

  • Magnetosome biogenesis entails the invagination of the magnetosome membrane, recruitment of specific proteins, iron transport and redox-controlled biomineralization of magnetite crystals; magnetosomes are then assembled and positioned into well-ordered linear chains that are among the most complex structures seen in prokaryotic organisms.

  • Key functions of magnetosome biogenesis are encoded by about 30 genes that are clustered in a genomic 'magnetosome island', although additional auxiliary functions are contributed by general cellular metabolic and regulatory pathways, including aerobic and anaerobic respiration.

  • A non-magnetotactic bacterium has recently been 'magnetized' through the heterologous expression of genes that encode the magnetosome biogenesis pathway, which is a proof-of-principle demonstration that non-magnetotactic bacteria that are more facile for laboratory investigation could be 'magnetized' to provide new models for genetic dissection and synthetic biology.

  • Bacterial magnetosomes are promising nanomaterials for various bioremediation, biomedical and bionanotechnological applications.

Abstract

Magnetotactic bacteria derive their magnetic orientation from magnetosomes, which are unique organelles that contain nanometre-sized crystals of magnetic iron minerals. Although these organelles have evident potential for exciting biotechnological applications, a lack of genetically tractable magnetotactic bacteria had hampered the development of such tools; however, in the past decade, genetic studies using two model Magnetospirillum species have revealed much about the mechanisms of magnetosome biogenesis. In this Review, we highlight these new insights and place the molecular mechanisms of magnetosome biogenesis in the context of the complex cell biology of Magnetospirillum spp. Furthermore, we discuss the diverse properties of magnetosome biogenesis in other species of magnetotactic bacteria and consider the value of genetically 'magnetizing' non-magnetotactic bacteria. Finally, we discuss future prospects for this highly interdisciplinary and rapidly advancing field.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Overview of the mechanisms and genetics of magnetosome biogenesis.
Figure 2: Magnetosome membrane invagination and protein recruitment.
Figure 3: Biomineralization of magnetite crystals.
Figure 4: Magnetosome chain assembly, positioning and segregation.
Figure 5: Diversity and genetic engineering of magnetosomes.

Similar content being viewed by others

References

  1. Lefévre, C. T. et al. Comparative genomic analysis of magnetotactic bacteria from the Deltaproteobacteria provides new insights into magnetite and greigite magnetosome genes required for magnetotaxis. Environ. Microbiol. 15, 2712–2735 (2013). An article that describes the discovery of a novel and conserved set of magnetosome ( mad ) genes in diverse bacteria.

    PubMed  Google Scholar 

  2. Kolinko, S., Richter, M., Glöckner, F.-O., Brachmann, A. & Schüler, D. Single-cell genomics reveals potential for magnetite and greigite biomineralization in an uncultivated multicellular magnetotactic prokaryote. Environ. Microbiol. Rep. 6, 524–531 (2014).

    CAS  PubMed  Google Scholar 

  3. Kolinko, S., Richter, M., Glöckner, F.-O., Brachmann, A. & Schüler, D. Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes. Environ. Microbiol. 18, 21–37 (2015). References 3 and 114 use complementary approaches to analyse the genomes of uncultured giant magnetotactic bacteria, discovering novel genes that are probably involved in the biogenesis and cellular organization of bullet-shaped magnetosomes.

    PubMed  Google Scholar 

  4. Kolinko, S. et al. Clone libraries and single cell genome amplification reveal extended diversity of uncultivated magnetotactic bacteria from marine and freshwater environments. Environ. Microbiol. 15, 1290–1301 (2013).

    CAS  PubMed  Google Scholar 

  5. Kolinko, S. et al. Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environ. Microbiol. 14, 1709–1721 (2012).

    CAS  PubMed  Google Scholar 

  6. Lin, W., Li, J. & Pan, Y. Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl. Environ. Microbiol. 78, 668–675 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Lin, W. & Pan, Y. A putative greigite-type magnetosome gene cluster from the candidate phylum Latescibacteria. Environ. Microbiol. Rep. 7, 237–242 (2015).

    CAS  PubMed  Google Scholar 

  8. Komeili, A. Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiol. Rev. 36, 232–255 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Guo, F. F. et al. Magnetosomes eliminate intracellular reactive oxygen species in Magnetospirillum gryphiswaldense MSR-1. Environ. Microbiol. 14, 1722–1729 (2012).

    CAS  PubMed  Google Scholar 

  10. Bellini, S. Ulteriori Studi Sui “Batteri Magnetosensibili.” (Pavia, 1963).

    Google Scholar 

  11. Blakemore, R. P. Magnetotactic bacteria. Science 190, 377–379 (1975). The first report of magnetosomes and the first contemporary report of magnetotactic bacteria.

    CAS  PubMed  Google Scholar 

  12. Faivre, D. & Schüler, D. Magnetotactic bacteria and magnetosomes. Chem. Rev. 108, 4875–4898 (2008).

    CAS  PubMed  Google Scholar 

  13. Bazylinski, D. & Frankel, R. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2, 217–230 (2004).

    CAS  PubMed  Google Scholar 

  14. Bazylinski, D. A., Lefévre, C. T. & Lower, B. H. in Nanomicrobiology (eds Barton, L. L., Bazylinski, D. A. & Xu, H.) 39–74 (Springer, 2014).

    Google Scholar 

  15. Lefévre, C. T. & Wu, L.-F. Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol. 21, 534–543 (2013).

    PubMed  Google Scholar 

  16. Lefévre, C. T. & Bazylinski, D. A. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol. Mol. Biol. Rev. 77, 497–526 (2013).

    PubMed  PubMed Central  Google Scholar 

  17. Grünberg, K., Wawer, C., Tebo, B. M. & Schüler, D. A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Appl. Environ. Microbiol. 67, 4573–4582 (2001).

    PubMed  PubMed Central  Google Scholar 

  18. Grünberg, K. et al. Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70, 1040–1050 (2004). Together with reference 17, this study describes the identification of magnetosome-associated proteins and the discovery of magnetosome- associated gene clusters.

    PubMed  PubMed Central  Google Scholar 

  19. Okuda, Y., Denda, K. & Fukumori, Y. Cloning and sequencing of a gene encoding a new member of the tetratricopeptide protein family from magnetosomes of Magnetospirillum magnetotacticum. Gene 171, 99–102 (1996).

    CAS  PubMed  Google Scholar 

  20. Arakaki, A., Webbs, J. & Matsunaga, T. A novel protein tightly bound to bacterial magnetite particles in Magnetospirillum magnetotacticum strain AMB-1. J. Biol. Chem. 278, 8745–8750 (2003).

    CAS  PubMed  Google Scholar 

  21. Fukuda, Y., Okamura, Y., Takeyama, H. & Matsunaga, T. Dynamic analysis of a genomic island in Magnetospirillum sp. strain AMB-1 reveals how magnetosome synthesis developed. FEBS Lett. 580, 801–812 (2006).

    CAS  PubMed  Google Scholar 

  22. Ullrich, S., Kube, M., Schübbe, S., Reinhardt, R. & Schüler, D. 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 (2005). This study describes the molecular structure and genetic instability of the MAI.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Dobrindt, U., Hochhut, B., Hentschel, U. & Hacker, J. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2, 414–424 (2004).

    CAS  PubMed  Google Scholar 

  24. Murat, D., Quinlan, A., Vali, H. & Komeili, A. Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc. Natl Acad. Sci. USA 107, 5593–5598 (2010). A seminal genetic study that shows the step-wise formation of magnetosomes and assigns genes to each step of biogenesis.

    CAS  PubMed  Google Scholar 

  25. Rong, C. et al. FeoB2 functions in magnetosome formation and oxidative stress protection in Magnetospirillum gryphiswaldense strain MSR-1. J. Bacteriol. 194, 3972–3976 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Scheffel, A., Gärdes, A., Grünberg, K., Wanner, G. & Schüler, D. 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 (2008).

    CAS  PubMed  Google Scholar 

  27. Lohsse, A. et al. Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense: the mamAB operon is sufficient for magnetite biomineralization. PLoS ONE 6, e25561 (2011). An extensive genetic study that shows that all of the essential functions for magnetosome formation are confined to the mamAB operon, whereas large regions of the magnetosome island are not required for magnetosome biogenesis.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Raschdorf, O., Müller, F. D., Pósfai, M., Plitzko, J. M. & Schüler, D. The magnetosome proteins MamX, MamZ and MamH are involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. Mol. Microbiol. 89, 872–886 (2013).

    CAS  PubMed  Google Scholar 

  29. Quinlan, A., Murat, D., Vali, H. & Komeili, A. The HtrA/DegP family protease MamE is a bifunctional protein with roles in magnetosome protein localization and magnetite biomineralization. Mol. Microbiol. 80, 1075–1087 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Draper, O. et al. MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Mol. Microbiol. 82, 342–354 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Rioux, J.-B. et al. A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island. PLoS ONE 5, e9151 (2010).

    PubMed  PubMed Central  Google Scholar 

  32. Gorby, Y. A., Beveridge, T. J. & Blakemore, R. Characterization of the bacterial magnetosome membrane. J. Bacteriol. 170, 834–841 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Balkwill, D., Maratea, D. & Blakemore, R. P. Ultrastructure of a magnetotactic spirillum. J. Bacteriol. 141, 1399–1408 (1980). Together with reference 32, this paper represents the first detailed study of the ultrastructure and composition of the magnetosome membrane.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Komeili, A., Li, Z., Newman, D. K. & Jensen, G. J. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311, 242–245 (2006).

    CAS  PubMed  Google Scholar 

  35. Katzmann, E., Scheffel, A., Gruska, M., Plitzko, J. M. & Schüler, D. Loss of the actin-like protein MamK has pleiotropic effects on magnetosome formation and chain assembly in Magnetospirillum gryphiswaldense. Mol. Microbiol. 77, 208–224 (2010).

    CAS  PubMed  Google Scholar 

  36. Cornejo, E., Subramanian, P., Li, Z., Jensen, G. J. & Komeili, A. Dynamic remodeling of the magnetosome membrane is triggered by the initiation of biomineralization. mBio 7, e01898–15 (2016).

    PubMed  PubMed Central  Google Scholar 

  37. Raschdorf, O. et al. Genetic and ultrastructural analysis reveals the key players and initial steps of bacterial magnetosome membrane biogenesis. PLoS Genet. 12, e1006101 (2016).

    PubMed  PubMed Central  Google Scholar 

  38. Scheffel, A. et al. An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440, 110–114 (2006). References 34 and 38 are pioneering studies that report the independent discoveries of a novel bacterial cytoskeletal structure that organizes magnetosome chains in Magnetospirillum spp. cells.

    CAS  PubMed  Google Scholar 

  39. Komeili, A., Vali, H., Beveridge, T. J. & Newman, D. K. Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc. Natl Acad. Sci. USA 101, 3839–3844 (2004). This study describes the first genetic analysis of a magnetosome protein.

    CAS  PubMed  Google Scholar 

  40. Faivre, D., Böttger, L. H., Matzanke, B. F. & Schüler, D. 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 (2007).

    CAS  PubMed  Google Scholar 

  41. Sweitzer, S. M. & Hinshaw, J. E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021–1029 (1998).

    CAS  PubMed  Google Scholar 

  42. Ford, M. G. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361–366 (2002).

    CAS  PubMed  Google Scholar 

  43. Uebe, R. et al. 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. Mol. Microbiol. 82, 818–835 (2011).

    CAS  PubMed  Google Scholar 

  44. Tanaka, M., Arakaki, A. & Matsunaga, T. Identification and functional characterization of liposome tubulation protein from magnetotactic bacteria. Mol. Microbiol. 76, 480–488 (2010).

    CAS  PubMed  Google Scholar 

  45. Kozlov, M. M. et al. Mechanisms shaping cell membranes. Curr. Opin. Cell Biol. 29, 53–60 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Faini, M., Beck, R., Wieland, F. T. & Briggs, J. A. Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol. 23, 279–288 (2013).

    CAS  PubMed  Google Scholar 

  47. Tanaka, M. et al. Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6, 5234–5247 (2006).

    CAS  PubMed  Google Scholar 

  48. Borg, S., Hofmann, J., Pollithy, A., Lang, C. & Schüler, D. New vectors for chromosomal integration enable high-level constitutive or inducible magnetosome expression of fusion proteins in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 80, 2609–2616 (2014).

    PubMed  PubMed Central  Google Scholar 

  49. Taoka, A. et al. Spatial localizations of Mam22 and Mam12 in the magnetosomes of Magnetospirillum magnetotacticum. J. Bacteriol. 188, 3805–3812 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Lang, C. & Schüler, D. Expression of green fluorescent protein fused to magnetosome proteins in microaerophilic magnetotactic bacteria. Appl. Environ. Microbiol. 74, 4944–4953 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Taoka, A. et al. A magnetosome-associated cytochrome MamP is critical for magnetite crystal growth during the exponential growth phase. FEMS Microbiol. Lett. 358, 21–29 (2014).

    CAS  PubMed  Google Scholar 

  52. Zeytuni, N. et al. Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly. Proc. Natl Acad. Sci. USA 108, E480–E487 (2011).

    CAS  PubMed  Google Scholar 

  53. Yamamoto, D. et al. Visualization and structural analysis of the bacterial magnetic organelle magnetosome using atomic force microscopy. Proc. Natl Acad. Sci. USA 107, 9382–9387 (2010).

    CAS  PubMed  Google Scholar 

  54. Nguyen, H. V. et al. A protein–protein interaction in magnetosomes: TPR protein MamA interacts with an Mms6 protein. Biochem. Biophys. Rep. 7, 39–44 (2016).

    PubMed  PubMed Central  Google Scholar 

  55. Lohsse, A. et al. Genetic dissection of the mamAB and mms6 operons reveals a gene set essential for magnetosome biogenesis in Magnetospirillum gryphiswaldense. J. Bacteriol. 196, 2658–2669 (2014). A comprehensive genetic analysis of the MAI, which identified a minimal gene set required for magnetite biomineralization.

    PubMed  PubMed Central  Google Scholar 

  56. Kashyap, S. et al. Visualization of iron-binding micelles in acidic recombinant biomineralization protein, MamC. J. Nanomater. 2014, 320124 (2014).

    Google Scholar 

  57. Valverde-Tercedor, C. et al. Subcellular localization of the magnetosome protein MamC in the marine magnetotactic bacterium Magnetococcus marinus strain MC-1 using immunoelectron microscopy. Arch. Microbiol. 196, 481–488 (2014).

    CAS  PubMed  Google Scholar 

  58. Arakaki, A., Yamagishi, A., Fukuyo, A., Tanaka, M. & Matsunaga, T. Co-ordinated functions of Mms proteins define the surface structure of cubo-octahedral magnetite crystals in magnetotactic bacteria. Mol. Microbiol. 93, 554–567 (2014).

    CAS  PubMed  Google Scholar 

  59. Tanaka, M., Mazuyama, E., Arakaki, A. & Matsunaga, T. Mms6 protein regulates crystal morphology during nano-sized magnetite biomineralization in vivo. J. Biol. Chem. 286, 6386–6392 (2011).

    CAS  PubMed  Google Scholar 

  60. Wang, L. et al. 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 (2012).

    PubMed  Google Scholar 

  61. Rawlings, A. E. et al. Self-assembled MmsF proteinosomes control magnetite nanoparticle formation in vitro. Proc. Natl Acad. Sci. USA 111, 16094–16099 (2014).

    CAS  PubMed  Google Scholar 

  62. Faivre, D. et al. Geochemical properties of inorganic magnetite nanocrystals. Waterrock Interac. 11, 1199–1202 (2004).

    Google Scholar 

  63. Schüler, D. & Baeuerlein, E. Iron-limited growth and kinetics of iron uptake in Magnetospirilum gryphiswaldense. Arch. Microbiol. 166, 301–307 (1996).

    PubMed  Google Scholar 

  64. Schüler, D. & Baeuerlein, E. Dynamics of iron uptake and Fe3O4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J. Bacteriol. 180, 159–162 (1998).

    PubMed  PubMed Central  Google Scholar 

  65. Flies, C. B. et al. Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol. Ecol. 52, 185–195 (2005).

    CAS  PubMed  Google Scholar 

  66. Rahn-Lee, L. & Komeili, A. The magnetosome model: insights into the mechanisms of bacterial biomineralization. Front. Microbiol. 4, 352 (2013).

    PubMed  PubMed Central  Google Scholar 

  67. Frankel, R., Papaefthymiou, G. C., Blakemore, R. P. & O'Brian, W. Fe3O4 precipitation in magnetotactic bacteria. Biochim. Biophys. Acta 763, 147–159 (1983).

    CAS  Google Scholar 

  68. Dubbels, B. et al. Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1. Microbiology 150, 2921–2945 (2004).

    Google Scholar 

  69. Paoletti, L. C. & Blakemore, R. P. Hydroxamate production by Aquaspirillum magnetotacticum. J. Bacteriol. 167, 73–76 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Calugay, R. J. et al. Catechol siderophore excretion by magnetotactic bacterium Magnetospirillum magneticum AMB-1. J. Biosci. Bioeng. 101, 445–447 (2006).

    CAS  PubMed  Google Scholar 

  71. Uebe, R. et al. Deletion of a fur-like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense. J. Bacteriol. 192, 4192–4204 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Wang, Q. et al. Iron response regulator protein IrrB in Magnetospirillum gryphiswaldense MSR-1 helps control iron/oxygen balance, oxidative stress tolerance and magnetosome formation. Appl. Environ. Microbiol. 81, 8044–8053 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Qi, L. et al. Fur in Magnetospirillum gryphiswaldense influences magnetosomes formation and directly regulates the genes involved in iron and oxygen metabolism. PLoS ONE 7, e29572 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Rong, C. et al. Ferrous iron transport protein B gene (feoB1) plays an accessory role in magnetosome formation in Magnetospirillum gryphiswaldense strain MSR-1. Res. Microbiol. 159, 530–536 (2008).

    CAS  PubMed  Google Scholar 

  75. Zeytuni, N. et al. Bacterial magnetosome biomineralization — a novel platform to study molecular mechanisms of human CDF-related type-II diabetes. PLoS ONE 9, e97154 (2014).

    PubMed  PubMed Central  Google Scholar 

  76. Zeytuni, N. et al. Cation diffusion facilitators transport initiation and regulation is mediated by cation induced conformational changes of the cytoplasmic domain. PLoS ONE 9, e92141 (2014).

    PubMed  PubMed Central  Google Scholar 

  77. Uebe, R., Henn, V. & Schüler, D. The MagA protein of magnetospirilla is not involved in bacterial magnetite biomineralization. J. Bacteriol. 194, 1018–1023 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Li, Y. et al. Cytochrome cd 1 nitrite reductase NirS is involved in anaerobic magnetite biomineralization in Magnetospirillum gryphiswaldense and requires NirN for proper d1 heme assembly. J. Bacteriol. 195, 4297–4309 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Li, Y., Katzmann, E., Borg, S. & Schüler, D. The periplasmic nitrate reductase Nap is required for anaerobic growth and involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. J. Bacteriol. 194, 4847–4856 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Li, Y., Raschdorf, O., Silva, K. T. & Schüler, D. The terminal oxidase cbb 3 functions in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. J. Bacteriol. 196, 2552–2562 (2014).

    PubMed  PubMed Central  Google Scholar 

  81. Katzmann, E. et al. Analysis of magnetosome chains in magnetotactic bacteria by magnetic measurements and automated image analysis of electron micrographs. Appl. Environ. Microbiol. 79, 7755–7762 (2013). Together with reference 88, references 79–81 provide the first genetic evidence that oxic and anoxic respiration are involved in redox control during magnetite biomineralization.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Moisescu, C., Ardelean, I. I. & Benning, L. G. The effect and role of environmental conditions on magnetosome synthesis. Front. Microbiol. 5, 49 (2014).

    PubMed  PubMed Central  Google Scholar 

  83. Heyen, U. & Schüler, D. Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl. Microbiol. Biotechnol. 61, 536–544 (2003). This study describes the first detailed analysis and optimization of conditions for fermenter-scale cultivation of magnetotactic bacteria and magnetosome production.

    CAS  PubMed  Google Scholar 

  84. Suzuki, T., Okamura, Y., Calugay, R. J., Takeyama, H. & Matsunaga, T. Global gene expression analysis of iron-inducible genes in Magnetospirillum magneticum AMB-1. J. Bacteriol. 188, 2275–2279 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Schübbe, S. et al. Transcriptional organization and regulation of magnetosome operons in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 72, 5757–5765 (2006).

    PubMed  PubMed Central  Google Scholar 

  86. Wang, X. et al. Transcriptome analysis reveals physiological characteristics required for magnetosome formation in Magnetospirillum gryphiswaldense MSR-1. Environ. Microbiol. Rep. 8, 371–381 (2016).

    CAS  PubMed  Google Scholar 

  87. Zhang, C. et al. Two bifunctional enzymes with ferric reduction ability play complementary roles during magnetosome synthesis in Magnetospirillum gryphiswaldense MSR-1. J. Bacteriol. 195, 876–885 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Li, Y. et al. The oxygen sensor MgFnr controls magnetite biomineralization by regulation of denitrification in Magnetospirillum gryphiswaldense. BMC Microbiol. 14, 153 (2014).

    PubMed  PubMed Central  Google Scholar 

  89. Siponen, M. I., Adryanczyk, G., Ginet, N., Arnoux, P. & Pignol, D. Magnetochrome: a c-type cytochrome domain specific to magnetotatic bacteria. Biochem. Soc. Trans. 40, 1319–1323 (2012).

    CAS  PubMed  Google Scholar 

  90. Siponen, M. I. et al. Structural insight into magnetochrome-mediated magnetite biomineralization. Nature 502, 681–684 (2013).

    CAS  PubMed  Google Scholar 

  91. Jones, S. R. et al. Genetic and biochemical investigations of the role of MamP in redox control of iron biomineralization in Magnetospirillum magneticum. Proc. Natl Acad. Sci. USA 112, 3904–3909 (2015). References 90–91 describe the structure and function of the novel magnetochrome domain in Fe2+ oxidation and magnetite biomineralization.

    CAS  PubMed  Google Scholar 

  92. Faivre, D. & Godec, T. U. From bacteria to mollusks: the principles underlying the biomineralization of iron oxide materials. Angew. Chem. Int. Ed Engl. 54, 4728–4747 (2015).

    CAS  PubMed  Google Scholar 

  93. Murat, D. et al. The magnetosome membrane protein, MmsF, is a major regulator of magnetite biomineralization in Magnetospirillum magneticum AMB-1. Mol. Microbiol. 85, 684–699 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Yang, W. et al. mamO and mamE genes are essential for magnetosome crystal biomineralization in Magnetospirillum gryphiswaldense MSR-1. Res. Microbiol. 161, 701–705 (2010).

    CAS  PubMed  Google Scholar 

  95. Hershey, D. M. et al. Magnetite biomineralization in Magnetospirillum magneticum is regulated by a switch-like behavior in the HtrA protease MamE. J.Biol. Chem, http://dx.doi.org/10.1074/jbc.M116.731000 (2016).

  96. Hershey, D. M. et al. MamO is a repurposed serine protease that promotes magnetite biomineralization through direct transition metal binding in magnetotactic bacteria. PLoS Biol. 14, e1002402 (2016).

    PubMed  PubMed Central  Google Scholar 

  97. Kashyap, S., Woehl, T. J., Liu, X., Mallapragada, S. K. & Prozorov, T. Nucleation of iron oxide nanoparticles mediated by Mms6 protein in situ. ACS Nano 8, 9097–9106 (2014).

    CAS  PubMed  Google Scholar 

  98. Arakaki, A., Masuda, F., Amemiya, Y., Tanaka, T. & Matsunaga, T. 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 (2010).

    CAS  PubMed  Google Scholar 

  99. Bazylinski, D. A. Structure and function of the bacterial magnetosome. ASM News 61, 337–343 (1995).

    Google Scholar 

  100. Klumpp, S. & Faivre, D. Interplay of magnetic interactions and active movements in the formation of magnetosome chains. PLoS ONE 7, e33562 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Schübbe, S. et al. Characterization of a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J. Bacteriol. 185, 5779–5790 (2003). This article reports the discovery of the genomic MAI.

    PubMed  PubMed Central  Google Scholar 

  102. Ozyamak, E., Kollman, J., Agard, D. A. & Komeili, A. The bacterial actin MamK: in vitro assembly behavior and filament architecture. J. Biol. Chem. 288, 4265–4277 (2013).

    CAS  PubMed  Google Scholar 

  103. Sonkaria, S. et al. Insight into the assembly properties and functional organisation of the magnetotactic bacterial actin-like homolog, MamK. PLoS ONE 7, e34189 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Abreu, N. et al. Interplay between two bacterial actin homologs, MamK and MamK-Like, is required for the alignment of magnetosome organelles in Magnetospirillum magneticum AMB-1. J. Bacteriol. 196, 3111–3121 (2014).

    PubMed  PubMed Central  Google Scholar 

  105. Pradel, N., Santini, C., Bernadac, A., Fukumori, Y. & Wu, L. Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proc. Natl Acad. Sci. USA 103, 17485–17489 (2006).

    CAS  PubMed  Google Scholar 

  106. Ozyamak, E., Kollman, J. M. & Komeili, A. Bacterial actins and their diversity. Biochemistry 52, 6928–6939 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Katzmann, E. et al. Magnetosome chains are recruited to cellular division sites and split by asymmetric septation. Mol. Microbiol. 82, 1316–1329 (2011). This study demonstrates that magnetotactic bacteria use dedicated mechanisms for intracellular positioning, division and partitioning of magnetosomes.

    PubMed  Google Scholar 

  108. Löwe, J. & Amos, L. A. Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochem. Cell Biol. 41, 323–329 (2009).

    PubMed  Google Scholar 

  109. Scheffel, A. & Schüler, D. 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 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Pan, W., Xie, C. & Lv, J. Screening for the interacting partners of the proteins MamK and MamJ by two-hybrid genomic DNA library of Magnetospirillum magneticum AMB-1. Curr. Microbiol. 64, 515–523 (2012).

    CAS  PubMed  Google Scholar 

  111. Philippe, N. & Wu, L.-F. 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 (2010).

    CAS  PubMed  Google Scholar 

  112. Zhu, X. et al. Angle sensing in magnetotaxis of Magnetospirillum magneticum AMB-1. Integr. Biol. (Camb.) 6, 706–713 (2014).

    CAS  Google Scholar 

  113. Lin, W. et al. Genomic insights into the uncultured genus 'Candidatus Magnetobacterium' in the phylum Nitrospirae. ISME J. 8, 2463–2477 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Staniland, S. S., Moisescu, C. & Benning, L. G. Cell division in magnetotactic bacteria splits magnetosome chain in half. J. Basic Microbiol. 50, 392–396 (2010).

    CAS  PubMed  Google Scholar 

  115. Lin, W. & Pan, Y. Snapping magnetosome chains by asymmetric cell division in magnetotactic bacteria. Mol. Microbiol. 82, 1301–1304 (2011).

    CAS  PubMed  Google Scholar 

  116. Adams, D. W. & Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7, 642–653 (2009).

    CAS  PubMed  Google Scholar 

  117. Jogler, C. et al. Toward cloning of the magnetotactic metagenome: identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl. Environ. Microbiol. 75, 3972–3979 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Richter, M. et al. 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 (2007). This study describes the in silico identification of gene sets that are shared by magnetotactic Alphaproteobacteria.

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Ding, Y. et al. Deletion of the ftsZ-like gene results in the production of superparamagnetic magnetite magnetosomes in Magnetospirillum gryphiswaldense. J. Bacteriol. 192, 1097–1105 (2010).

    CAS  PubMed  Google Scholar 

  120. Müller, F. D. et al. The FtsZ-like protein FtsZm of Magnetospirillum gryphiswaldense likely interacts with its generic homolog and is required for biomineralization under nitrate deprivation. J. Bacteriol. 196, 650–659 (2014).

    PubMed  PubMed Central  Google Scholar 

  121. Pósfai, M., Lefévre, C. T., Trubitsyn, D., Bazylinski, D. A. & Frankel, R. B. Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front. Microbiol. 4, 344 (2013).

    PubMed  PubMed Central  Google Scholar 

  122. Lin, W., Bazylinski, D. A., Xiao, T., Wu, L.-F. & Pan, Y. Life with compass: diversity and biogeography of magnetotactic bacteria. Environ. Microbiol. 16, 2646–2658 (2014).

    CAS  PubMed  Google Scholar 

  123. Lefévre, C. T. et al. Monophyletic origin of magnetotaxis and the first magnetosomes. Environ. Microbiol. 15, 2267–2274 (2013).

    PubMed  Google Scholar 

  124. Rahn-Lee, L. et al. A genetic strategy for probing the functional diversity of magnetosome formation. PLoS Genet. 11, e1004811 (2015).

    PubMed  PubMed Central  Google Scholar 

  125. Lohsse, A. et al. Overproduction of magnetosomes by genomic amplification of biosynthetic gene clusters in a magnetotactic bacterium. Appl. Environ. Microbiol. 82, 3032–3041 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Abreu, F. et al. Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria. ISME J. 5, 1634–1640 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Lefévre, C. T. et al. A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 334, 1720–1723 (2011). This study describes the first isolation and cultivation of a magnetotactic bacterium that forms greigite magnetosomes, as well as the identification of gene clusters that putatively control greigite biomineralization.

    PubMed  Google Scholar 

  128. Kirschvink, J. L., Walker, M. M. & Diebel, C. E. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11, 462–467 (2001).

    CAS  PubMed  Google Scholar 

  129. Kolinko, I. et al. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat. Nanotechnol. 9, 193–197 (2014). Pioneering paper that shows that magnetosome biogenesis can be genetically transferred to non-magnetotactic bacteria.

    CAS  PubMed  Google Scholar 

  130. Jogler, C. et al. Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proc. Natl Acad. Sci. USA 108, 1134–1139 (2011). First report to show that mam gene clusters are also conserved in the MAI of deep-branching uncultivated magnetotactic bacteria.

    CAS  PubMed  Google Scholar 

  131. Lefévre, C. T. et al. Insight into the evolution of magnetotaxis in Magnetospirillum spp., based on mam gene phylogeny. Appl. Environ. Microbiol. 78, 7238–7248 (2012).

    PubMed  PubMed Central  Google Scholar 

  132. Lefévre, C. T., Bernadac, A., Yu-Zhang, K., Pradel, N. & Wu, L.-F. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ. Microbiol. 11, 1646–1657 (2009).

    PubMed  Google Scholar 

  133. Lefévre, C. T., Frankel, R. B., Pósfai, M., Prozorov, T. & Bazylinski, D. A. Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ. Microbiol. 13, 2342–2350 (2011).

    PubMed  Google Scholar 

  134. Lefévre, C. T. et al. Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J. 6, 440–450 (2012).

    PubMed  Google Scholar 

  135. Goldhawk, D. E., Rohani, R., Sengupta, A., Gelman, N. & Prato, F. S. Using the magnetosome to model effective gene-based contrast for magnetic resonance imaging. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4, 378–388 (2012).

    CAS  PubMed  Google Scholar 

  136. Westmeyer, G. G. & Jasanoff, A. Genetically controlled MRI contrast mechanisms and their prospects in systems neuroscience research. Magn. Reson. Imaging 25, 1004–1010 (2007).

    PubMed  Google Scholar 

  137. Huang, H., Delikanli, S., Zeng, H., Ferkey, D. M. & Pralle, A. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nat. Nanotechnol. 5, 602–606 (2010).

    CAS  PubMed  Google Scholar 

  138. González, L. M., Ruder, W. C., Mitchell, A. P., Messner, W. C. & LeDuc, P. R. Sudden motility reversal indicates sensing of magnetic field gradients in Magnetospirillum magneticum AMB-1 strain. ISME J. 9, 1399–1409 (2015).

    PubMed  Google Scholar 

  139. Frankel, R. B., Bazylinski, D. A., Johnson, M. S. & Taylor, B. L. Magneto-aerotaxis in marine coccoid bacteria. Biophys. J. 73, 994–1000 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Chen, C., Ma, Q., Jiang, W. & Song, T. Phototaxis in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1 is independent of magnetic fields. Appl. Microbiol. Biotechnol. 90, 269–275 (2011).

    CAS  PubMed  Google Scholar 

  141. Simmons, S. L., Bazylinski, D. A. & Edwards, K. J. Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ. Microbiol. 9, 2162–2174 (2007).

    CAS  PubMed  Google Scholar 

  142. Popp, F., Armitage, J. P. & Schüler, D. Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway. Nat. Commun. 5, 5398 (2014). This study describes the detailed and quantitative analysis of the magnetotactic motility and behaviour of Magnetospirillum spp. cells and provides the first insights into the molecular mechanisms of magneto-aerotaxis.

    CAS  PubMed  Google Scholar 

  143. Lefévre, C. T. et al. Diversity of magneto-aerotactic behaviors and oxygen sensing mechanisms in cultured magnetotactic bacteria. Biophys. J. 107, 527–538 (2014).

    PubMed  PubMed Central  Google Scholar 

  144. Zhang, W.-J., Chen, C., Li, Y., Song, T. & Wu, L.-F. Configuration of redox gradient determines magnetotactic polarity of the marine bacteria MO-1. Environ. Microbiol. Rep. 2, 646–650 (2010).

    CAS  PubMed  Google Scholar 

  145. Porter, S. L., Wadhams, G. H. & Armitage, J. P. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 9, 153–165 (2011).

    CAS  PubMed  Google Scholar 

  146. Ginet, N. et al. Single-step production of a recyclable nanobiocatalyst for organophosphate pesticides biodegradation using functionalized bacterial magnetosomes. PLoS ONE 6, e21442 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Lang, C. & Schüler, D. Biogenic nanoparticles: production, characterization, and application of bacterial magnetosomes. J. Phys.: Condens. Matter 18, S2815–S2828 (2006).

    CAS  Google Scholar 

  148. Araujo, A. C. V., Abreu, F., Silva, K. T., Bazylinski, D. A. & Lins, U. Magnetotactic bacteria as potential sources of bioproducts. Mar. Drugs 13, 389–430 (2015).

    PubMed  PubMed Central  Google Scholar 

  149. Hergt, R. et al. Magnetic properties of bacterial magnetosomes as potential diagnostic and therapeutic tools. J. Magn. Magn. Mater. 293, 80–86 (2005).

    CAS  Google Scholar 

  150. Céspedes, E. et al. Bacterially synthesized ferrite nanoparticles for magnetic hyperthermia applications. Nanoscale 6, 12958–12970 (2014).

    PubMed  Google Scholar 

  151. Alphandéry, E., Guyot, F. & Chebbi, I. Preparation of chains of magnetosomes, isolated from Magnetospirillum magneticum strain AMB-1 magnetotactic bacteria, yielding efficient treatment of tumors using magnetic hyperthermia. Int. J. Pharm. 434, 444–452 (2012).

    PubMed  Google Scholar 

  152. Taukulis, R. et al. Magnetic iron oxide nanoparticles as MRI contrast agents — a comprehensive physical and theoretical study. Magnetohydrodynamics 51, 721–748 (2015).

    Google Scholar 

  153. Mériaux, S. et al. Magnetosomes, biogenic magnetic nanomaterials for brain molecular imaging with 17.2 T MRI scanner. Adv. Healthc. Mater. 4, 1076–1083 (2015).

    PubMed  Google Scholar 

  154. Lisy, M. R. et al. Fluorescent bacterial magnetic nanoparticles as bimodal contrast agents. Invest. Radiol. 42, 235–241 (2007).

    CAS  PubMed  Google Scholar 

  155. Schwarz, S. et al. Synthetic and biogenic magnetite nanoparticles for tracking of stem cells and dendritic cells. J. Magn. Magn. Mater. 321, 1533–1538 (2009).

    CAS  Google Scholar 

  156. Hartung, A. et al. Labeling of macrophages using bacterial magnetosomes and their characterization by magnetic resonance imaging. J. Magn. Magn. Mater. 311, 454–459 (2007).

    CAS  Google Scholar 

  157. Wacker, R. et al. Magneto immuno-PCR. A novel immunoassay based on biogenic magnetosome nanoparticles. Biochem. Biophys. Res. Commun. 357, 391–396 (2007).

    CAS  PubMed  Google Scholar 

  158. Ceyhan, B., Alhorn, P., Lang, C., Schüler, D. & Niemeyer, C. M. Semisynthetic biogenic magnetosome nanoparticles for the detection of proteins and nucleic acids. Small 2, 1251–1255 (2006).

    CAS  PubMed  Google Scholar 

  159. Yoshino, T. & Matsunaga, T. Efficient and stable display of functional proteins on bacterial magnetic particles using Mms13 as a novel anchor molecule. Appl. Environ. Microbiol. 72, 465–471 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Lang, C., Pollithy, A. & Schüler, D. Identification of promoters for efficient gene expression in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 75, 4206–4210 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Pollithy, A. et al. Magnetosome expression of functional camelid antibody fragments (nanobodies) in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 77, 6165–6171 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  162. Ohuchi, S. & Schüler, D. In vivo display of a multisubunit enzyme complex on biogenic magnetic nanoparticles. Appl. Environ. Microbiol. 75, 7734–7738 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Honda, T. et al. Novel designs of single-chain MHC I/peptide complex for the magnetosome display system. Protein Eng. Des. Sel. 28, 53–58 (2015).

    CAS  PubMed  Google Scholar 

  164. Sugamata, Y., Tanaka, T., Matsunaga, T. & Yoshino, T. Functional expression of an scFv on bacterial magnetic particles by in vitro docking. Biochem. Biophys. Res. Commun. 445, 1–5 (2014).

    CAS  PubMed  Google Scholar 

  165. Borg, S. et al. An intracellular nanotrap redirects proteins and organelles in live bacteria. mBio 6, e02117-14 (2015).

    PubMed  PubMed Central  Google Scholar 

  166. Borg, S., Rothenstein, D., Bill, J. & Schüler, D. Generation of multishell magnetic hybrid nanoparticles by encapsulation of genetically engineered and fluorescent bacterial magnetosomes with ZnO and SiO2 . Small 11, 4209–4217 (2015).

    CAS  PubMed  Google Scholar 

  167. Guo, F. et al. A novel rapid and continuous procedure for large-scale purification of magnetosomes from Magnetospirillum gryphiswaldense. Appl. Microbiol. Biotechnol. 90, 1277–1283 (2011).

    CAS  PubMed  Google Scholar 

  168. Silva, K. T. et al. Optimization of magnetosome production and growth by the magnetotactic vibrio Magnetovibrio blakemorei strain MV-1 through a statistics-based experimental design. Appl. Environ. Microbiol. 79, 2823–2827 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  169. Schüler, D. Formation of magnetosomes in magnetotactic bacteria. J. Mol. Microbiol. Biotechnol. 1, 79–86 (1999).

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank their co-workers and colleagues for helpful discussions. Work in the Schüler laboratory is supported by grants from the Human Frontier Science Program (HFSP), the Deutsche Forschungsgemeinschaft and the European Research Council (ERC).

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Bayreuth, Universitätsstraße 30, Bayreuth, 95447, Germany

    René Uebe & Dirk Schüler

Authors
  1. René Uebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk Schüler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Schüler.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information S1 (table) (PDF 155 kb)

PowerPoint slides

Glossary

Microoxic

A concentration of oxygen that is less than 21% and therefore lower than that found in the atmosphere.

Biomineralization

The process by which organisms form inorganic minerals.

Aerotaxis

Movement of an organism towards (positive) or away (negative) from oxygen.

Chemoreceptors

Proteins that detect certain chemical stimuli in the environment.

Genomic islands

Discrete genomic regions that can be transferred horizontally. These genomic regions typically encode several transposases and integrases to increase the rate of DNA turnover and are frequently associated with the adaptation of microorganisms to new environments.

Cation diffusion facilitator

(CDF). A ubiquitous family of proteins that transport divalent metal cations (such as Zn2+, Mn2+, Cd2+, Co2+ and Fe2+) using a proton or potassium antiport mechanism.

Tetratricopeptide repeat

(TPR). A structural motif of 34 degenerate amino acids that is often involved in the assembly of multiprotein complexes by mediating protein–protein interactions.

Landmark protein

Proteins that mark certain cellular regions (or structures) and that may direct the assembly of larger multiprotein complexes.

PDZ domain

A short (80–90 amino acids) protein domain that is often involved in organizing signalling complexes by forming protein–protein interactions with carboxy-terminal peptides. The name derives from the proteins in which the domain was first described: postsynaptic density protein 95 (PSD95), discs large homologue 1(Dlg1) and zonula occludens 1 (ZO-1).

Mössbauer spectroscopy

A spectroscopic technique that is based on the Mössbauer effect, which is the nearly recoil-free, resonant absorption and emission of gamma rays in solids.

Major facilitator superfamily

(MFS). A family of ubiquitous membrane proteins that transports sugars, oligosaccharides, amino acids, peptides, drugs, metal ions and oxyanions, either across an electrochemical (uniporter) or a chemiosmotic (symporter or antiporter) gradient.

Magnetic heating

The process of heat release by magnetic nanoparticles that are exposed to alternating magnetic fields.

Colloidal stability

The tendency of particles to remain suspended in solution.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uebe, R., Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nat Rev Microbiol 14, 621–637 (2016). https://doi.org/10.1038/nrmicro.2016.99

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro.2016.99

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology