Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bulletshaped magnetosomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 27, 2010, Pages 12263-12268

  Byrne, Meghan E ^a   Ball, David A ^b   Guerquin Kern, Jean Luc ^c,d   Rouiller, Isabelle ^e   Wu, Ting Di ^c,d   Downing, Kenneth H ^b   Vali, Hojatollah ^e   Komeili, Arash ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c INSERM   (France)

^d INSTITUT CURIE   (France)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Bacterial organelle; Biomineralization; Dynamic secondary ion mass spectroscopy; Magnetite; Magnetotactic bacteria

Indexed keywords

IRON; MAGNETITE; PHOSPHORUS;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL CELL; BIOMINERALIZATION; CELL GRANULE; CELL ORGANELLE; CELL ULTRASTRUCTURE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DESULFOVIBRIO; DESULFOVIBRIO MAGNETICUS; ELECTRON TOMOGRAPHY; MAGNETOSOME; MASS SPECTROMETRY; NANOIMAGING; PRIORITY JOURNAL; SPECIES; ULTRAMICROTOMY;

CRYOELECTRON MICROSCOPY; CRYSTALLIZATION; CYTOPLASMIC GRANULES; DESULFOVIBRIO; ELECTRON MICROSCOPE TOMOGRAPHY; FERROSOFERRIC OXIDE; IRON; MAGNETOSOMES; MICROSCOPY, ELECTRON, TRANSMISSION; MINERALS; PERIPLASM; PHOSPHORUS;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); DESULFOVIBRIO MAGNETICUS;

EID: 77955465482     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1001290107     Document Type: Article

References (33)

1. Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217-230.
2. Crookes-Goodson WJ, Slocik JM, Naik RR (2008) Bio-directed synthesis and assembly of nanomaterials. Chem Soc Rev 37:2403-2412.
3. Komeili A (2007) Molecular mechanisms of magnetosome formation. Annu Rev Biochem 76:351-366.
4. Gorby YA, Beveridge TJ, Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170:834-841.
5. Komeili A, Vali H, Beveridge TJ, Newman DK (2004) Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc Natl Acad Sci USA 101:3839-3844.
6. Schüler D, Baeuerlein E (1998) Dynamics of iron uptake and Fe3O4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180:159-162.
7. Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D (2005) A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J Bacteriol 187: 7176-7184.
8. Lins U, Freitas F, Keim CN, Farina M (2000) Electron spectroscopic imaging of magnetotactic bacteria: Magnetosome morphology and diversity. Microsc Microanal 6: 463-470.
9. Vali H, Kirschvink JL (1990) Observations of magnetosome organization, surface structure, and iron biomineralization of undescribed magnetic bacteria: Evolutionary speculations. Iron Biominerals, eds Frankel RB, Blakemore RP (Plenum Press, New York), pp 97-115.
10. Amman R, Peplies J, Schuler D (2007) Diversity and Taxonomy of Magnetotactic Bacteria. Microbiology Monographs (Springer, Berlin, Heidelberg), Vol 3, pp 25-36.
11. Sakaguchi T, Burgess JG, Matsunaga T (1993) Magnetite formation by a sulfate-reducing bacterium. Nature 365:47-49.
12. Sakaguchi T, Arakaki A, Matsunaga T (2002) Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. Int J Syst Evol Microbiol 52:215-221.
13. Kawaguchi R, et al. (1995) Phylogenetic analysis of a novel sulfate-reducing magnetic bacterium, RS-1, demonstrates its membership of the delta-Proteobacteria. FEMS Microbiol Lett 126:277-282.
14. Nakazawa H, et al. (2009) Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria. Genome Res 19: 1801-1808.
15. 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. J Colloid Interface Sci 343:65-70.
16. Sakaguchi T, Tsujimura N, Matsunaga T (1996) A novel method for isolation of magnetic bacteria without magnetic collection using magnetotaxis. J Microbiol Methods 26:139-145.
17. Posfai M, et al. (2006) Properties of intracellular magnetite crystals produced by Desulfovibrio magneticus strain RS-1. Earth Planet Sci Lett 249:444-455.
18. Schuler D, Uhl R, Bauerlein E (1995) A simple light-scattering method to assay magnetism in Magnetospirillum gryphiswaldense. FEMS Microbiol Lett 132:139-145.
19. Mandernack KW, Bazylinski DA, Shanks WC, 3rd, Bullen TD (1999) Oxygen and iron isotope studies of magnetite produced by magnetotactic bacteria. Science 285: 1892-1896.
20. Kürner J, Medalia O, Linaroudis AA, Baumeister W (2004) New insights into the structural organization of eukaryotic and prokaryotic cytoskeletons using cryoelectron tomography. Exp Cell Res 301:38-42.
21. Komeili A, Li Z, Newman DK, Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242-245.
22. Boxer SG, Kraft ML, Weber PK (2009) Advances in imaging secondary ion mass spectrometry for biological samples. Annu Rev Biophys 38:53-74.
23. Barton LL, Fauque GD (2009) Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 68:41-98.
24. Hensgens CMH, Santos H, Zhang C, Kruizinga WH, Hansen TA (1996) Electron-dense granules in Desulfovibrio gigas do not consist of inorganic triphosphate but of a glucose pentakis(diphosphate). Eur J Biochem 242:327-331.
25. Matsunaga T, Nemoto M, Arakaki A, Tanaka M (2009) Proteomic analysis of irregular, bullet-shaped magnetosomes in the sulphate-reducing magnetotactic bacterium Desulfovibrio magneticus RS-1. Proteomics 9:3341-3352.
26. Grünberg K, et al. (2004) Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl Environ Microbiol 70: 1040-1050.
27. Arakaki A, Webb J, Matsunaga T (2003) A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J Biol Chem 278: 8745-8750.
28. Murat D, Quinlan A, Vali H, Komeili A (2010) Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc Natl Acad Sci USA 107:5593-5598.
29. Amemiya Y, Arakaki A, Staniland SS, 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.
30. 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. J Bacteriol 190:377-386.
31. Hanzlik M, Winklhofer M, Petersen N (2002) Pulsed-field-remanence measurements on individual magnetotactic bacteria. J Magn Magn Mater 248:258-267.
32. Guerquin-Kern JL, Wu TD, Quintana C, Croisy A (2005) Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). Biochim Biophys Acta 1724:228-238.
33. Azari F, et al. (2008) Intracellular precipitation of hydroxyapatite mineral and implications for pathologic calcification. J Struct Biol 162:468-479.