Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function

Journal of Bacteriology

Volumn 189, Issue 13, 2007, Pages 4899-4910

  Richter, Michael ^a,c   Kube, Michael ^b   Bazylinski, Dennis A ^d   Lombardot, Thierry ^a   Glöckner, Frank Oliver ^a,c   Reinhardt, Richard ^b   Schüler, Dirk ^a,e  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c JACOBS UNIVERSITY BREMEN   (Germany)

^d UNIVERSITY OF NEVADA   (United States)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENETICS; BIOMINERALIZATION; CELL ORGANELLE; COMPLEX FORMATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC ANALYSIS; MAGNETIC FIELD; MAGNETISM; MAGNETOSOME; MAGNETOSPIRILLUM; MAGNETOSPIRILLUM GRYPHISWALDENSE; MAGNETOSPIRILLUM MAGNETOTACTICUM; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROKARYOTE;

BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMICS; MAGNETICS; MAGNETOSPIRILLUM; OPEN READING FRAMES; OPERON; PHYLOGENY;

ALPHAPROTEOBACTERIA; ARCHAEA; BACTERIA (MICROORGANISMS); MAGNETIC COCCUS MP17; MAGNETOSPIRILLUM; MAGNETOSPIRILLUM GRYPHISWALDENSE; MAGNETOSPIRILLUM MAGNETICUM AMB-1; MAGNETOSPIRILLUM MAGNETOTACTICUM MS-1; PROKARYOTA;

EID: 34347392111     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00119-07     Document Type: Article

References (45)

1. Alexandre, G., S. Greer-Phillips, and I. B. Zhulin. 2004. Ecological role of energy taxis in microorganisms. FEMS Microbiol. Rev. 28:113-126.
2. Amann, R., J. Peplies, and D. Schiller. 2006. Diversity and taxonomy of magnetotactic bacteria, pp. 25-36. In D. Schüler (ed.), Magnetoreception and magnetosomes in bacteria. Springer-Verlag, Berlin, Germany.
3. Arakaki, A., J. Webb, and T. Matsunaga. 2003. A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J. Biol. Chem. 278:8745-8750.
4. Badger, J. H., and G. J. Olsen. 1999. CRITICA: coding region identification tool invoking comparative analysis. Mol. Biol. Evol. 16:512-524.
5. Bazylinski, D. A., A. J. Dean, T. J. Williams, L. K. Long, S. L. Middleton, and B. L. Dubbels. 2004. Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch. Microbiol. 182:373-387.
6. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
7. Blakemore, R. P., D. Maratea, and R. S. Wolfe. 1979. Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J. Bacteriol. 140:720-729.
8. Delcher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641.
9. Felsenstein, J. 1989. PHYLIP, phylogeny inference package (version 3.2). Cladistics 5:164-166.
10. Forterre, P. 2002. A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet. 18:236-237.
11. Frankel, R. B. 2006. Aerotaxis, pp. 1-24. In D. Schüler (ed.), Magnetoreception and magnetosomes in bacteria. Springer-Verlag, Berlin, Germany.
12. Frankel, R. B., D. A. Bazylinski, M. S. Johnson, and B. L. Taylor. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophys. J. 73:994-1000.
13. Fukuda, Y., Y. Okamura, H. Takeyama, and T. Matsunaga. 2006. Dynamic analysis of a genomic island in Magnetospirillum sp. strain AMB-1 reveals how magnetosome synthesis developed. FEBS Lett. 80:801-812.
14. Galperin, M. Y., and E. V. Koonin. 2004. Conserved hypothetical proteins: prioritization of targets for experimental study. Nucleic Acids Res. 32:5452-5463.
15. Glöckner, F. O., M. Kube, M. Bauer, H. Teeling, T. Lombardot, W. Ludwig, D. Gade, A. Beck, K. Borzym, K. Heitmann, R. Rabus, H. Schlesner, R. Amann, and R. Reinhardt. 2003. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl. Acad. Sci. USA 100:8298-8303.
16. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202.
17. Grünberg, K., E. Müller, A. Otto, R. Reszka, D. Linder, M. Kube, R. Reinhardt, and D. Schüler. 2004. Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70:1040-1050.
18. Grünberg, K., C. Wawer, B. M. Tebo, and D. Schüler. 2001. A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Appl. Environ. Microbiol. 67:4573-4582.
19. Guo, F., H. Ou, and C. Zhang. 2003. ZCURVE: a new system for recognizing protein-coding genes in bacterial and archaeal genomes. Nucleic Acids Res. 31:1780-1789.
20. Komeili, A., H. Vali, T. J. Beveridge, and D. K. Newman. 2004. Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc. Natl. Acad. Sci. USA 101:3839-3844.
21. Komeili, A., Z. Li, D. K. Newman, and G. J. Jensen. 2006. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242-245.
22. Koonin, E. V., A. R. Mushegian, and P. Bork. 1996. Non-orthologous gene displacement. Trends Genet. 12:334-336.
23. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
24. Makarova, K. S., Y. I. Wolf, and E. V. Koonin. 2003. Potential genomic determinants of hyperthermophily. Trends Genet. 19:172-176.
25. Margolin, W. 2006. Bacterial division: another way to box in the ring. Curr. Biol. 16:881-884.
26. Martin, K. A., J. L. Siefert, S. Yerrapragada, Y. Lu, T. Z. McNeill, P. A. Moreno, G. M. Weinstock, W. R. Widger, and G. E. Fox. 2003. Cyanobacterial signature genes. Photosynth. Res. 75:211-221.
27. Matsunaga, T., Y. Okamura, Y. Fukuda, A. T. Wahyudi, Y. Murase, and H. Takeyama. 2005. Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res. 12:157-166.
28. Meldrum, F. C., S. Mann, B. R. Heywood, R. B. Frankel, and D. A. Bazylinski. 1993. Electron microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium. Proc. Biol. Sci. 251:231-236.
29. Meyer, F., A. Goesmann, A. C. McHardy, D. Bartels, T. Bekel, J. Clausen, J. Kalinowski, B. Linke, O. Rupp, R. Giegerich, and A. Pühler. 2003. GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 31:2187-2195.
30. Mulkidjanian, A. Y., E. V. Koonin, K. S. Makarova, S. L. Mekhedov, A. Sorokin, Y. I. Wolf, A. Dufresne, F. Partensky, H. Burd, D. Kaznadzey, R. Haselkorn, and M. Y. Galperin. 2006. The cyanobacterial genome core and the origin of photosynthesis. Proc. Natl. Acad. Sci. USA 103:13126-13131.
31. Osterman, A., and R. Overbeek. 2003. Missing genes in metabolic pathways: a comparative genomics approach. Curr. Opin. Chem. Biol. 7:238-251.
32. Pradel, N., C.-L. Santini, A. Bernadac, Y. Fukumori, and L.-F. Wu. 2006. Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proc. Natl. Acad. Sci. USA 103:17485-17489.
33. Quast, C. 2006. MicHanThi-design and implementation of a system for the prediction of gene functions in genome annotation projects. Ph.D. thesis. University of Bremen, Bremen, Germany.
34. Raymond, J., O. Zhaxybayeva, J. P. Gogarten, S. Y. Gerdes, and R. E. Blankenship. 2002. Whole genome analysis of photosynthetic prokaryotes. Science 298:1616-1620.
35. Rocap, G., F. W. Larimer, J. Lamerdin, S. Malfatti, P. Chain, N. A. Ahlgren, A. Arellano, M. Coleman, L. Hauser, W. R. Hess, Z. I. Johnson, M. Land, D. Lindell, A. F. Post, W. Regala, M. Shah, S. L. Shaw, C. Steglich, M. B. Sullivan, C. S. Ting, A. Tolonen, E. A. Webb, E. R. Zinser, and S. W. Chisholm. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042-1047.
36. Roman, D. G., A. Dancis, G. J. Anderson, and R. D. Klausner. 1993. The fission yeast ferric reductase gene frp1 + is required for ferric iron uptake and encodes a protein that is homologous to the gp91-phox subunit of the human NADPH phagocyte oxidoreductase. Mol. Cell. Biol. 13:4342-4350.
37. Scheffel, A., M. Gruska, D. Faivre, A. Linaroudis, P. Graumann, J. M. Plitzko, and D. Schüler. 2006. An acidic protein aligns magnetosomes along filamentous structure in magnetotactic bacteria. Nature 440:110-114.
38. Schleifer, K., D. Schüler, S. Spring, M. Weizenegger, R. Amann, W. Ludwig, and M. Köhler. 1991. The genus Magnetospirillum gen. nov. description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. Syst. Appl. Microbiol. 14:379-385.
39. Schübbe, S., M. Kube, A. Scheffel, C. Wawer, U. Heyen, A. Meyerdierks, M. H. Madkour, F. Mayer, R. Reinhardt, and D. Schüler. 2003. Characterization of a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J. Bacteriol. 185:5779-5790.
40. Siew, N., Y. Azaria, and D. Fischer. 2004. The ORFanage: an ORFan database. Nucleic Acids Res. 32:281-283.
41. Tanaka, M., Y. Okamura, A. Arakaki, T. Tanaka, H. Takeyama, and T. Matsunaga. 2006. Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6:5234-5247.
42. Ullrich, S., M. Kube, S. Schübbe, R. Reinhardt, and D. Schüler. 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.
43. Williams, T. J., C. L. Zhang, J. H. Scott, and D. A. Bazylinski. 2006. Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl. Environ. Microbiol. 72:1322-1329.
44. Wilson, G. A., N. Bertrand, Y. Patel, J. B. Hughes, E. J. Feil, and D. Field. 2005. Orphans as taxonomically restricted and ecologically important genes. Microbiology 151:2499-2501.
45. Zhulin, I. B., A. N. Nikolskaya, and M. Y. Galperin. 2003. Common extracellular sensory domains in transmembrane receptors for diverse signal transduction pathways in bacteria and archaea. J. Bacteriol. 185:285-294.