1887

Abstract

Magnetotactic bacteria (MTB) are widespread aquatic bacteria, and are a phylogenetically, physiologically and morphologically heterogeneous group, but they all have the ability to orientate and move along the geomagnetic field using intracellular magnetic organelles called magnetosomes. Isolation and cultivation of novel MTB are necessary for a comprehensive understanding of magnetosome formation and function in divergent MTB. In this study, we enriched a giant rod-shaped magnetotactic bacterium (strain GRS-1) from a freshwater pond in Kanazawa, Japan. Cells of strain GRS-1 were unusually large (~13×~8 µm). They swam in a helical trajectory towards the south pole of a bar magnet by means of a polar bundle of flagella. Another striking feature of GRS-1 was the presence of two distinct intracellular biomineralized structures: large electron-dense granules composed of calcium and long chains of magnetosomes that surround the large calcium granules. Phylogenetic analysis based on the 16S rRNA gene sequence revealed that this strain belongs to the and represents a new genus of MTB.

Funding
This study was supported by the:
  • MEXT KAKENHI (Award 24117007)
  • JSPS KAKENHI (Award 25850051)
  • Institute for Fermentation, Osaka
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.078717-0
2014-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/10/2226.html?itemId=/content/journal/micro/10.1099/mic.0.078717-0&mimeType=html&fmt=ahah

References

  1. Bazylinski D. A., Frankel R. B. ( 2004). Magnetosome formation in prokaryotes. Nat Rev Microbiol 2:217–230 [View Article][PubMed]
    [Google Scholar]
  2. Blakemore R. ( 1975). Magnetotactic bacteria. Science 190:377–379 [View Article][PubMed]
    [Google Scholar]
  3. Butler R. F., Banerjee S. K. ( 1975). Theoretical single-domain grain size range in magnetite and titanomagnetite. J Geophys Res 80:4049–4058 [View Article]
    [Google Scholar]
  4. Byrne M. E., Ball D. A., Guerquin-Kern J.-L., Rouiller I., Wu T.-D., Downing K. H., Vali H., Komeili A. ( 2010). Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes. Proc Natl Acad Sci U S A 107:12263–12268 [View Article][PubMed]
    [Google Scholar]
  5. Faivre D., Schüler D. ( 2008). Magnetotactic bacteria and magnetosomes. Chem Rev 108:4875–4898 [View Article][PubMed]
    [Google Scholar]
  6. Gorby Y. A., Beveridge T. J., Blakemore R. P. ( 1988). Characterization of the bacterial magnetosome membrane. J Bacteriol 170:834–841[PubMed]
    [Google Scholar]
  7. Hall T. A. ( 1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  8. Isambert A., Menguy N., Larquet E., Guyot F., Valet J. P. ( 2007). Transmission electron microscopy study of magnetites in a freshwater population of magnetotactic bacteria. Am Miner 92:621–630 [View Article]
    [Google Scholar]
  9. Keim C. N., Solórzano G., Farina M., Lins U. ( 2005). Intracellular inclusions of uncultured magnetotactic bacteria. Int Microbiol 8:111–117[PubMed]
    [Google Scholar]
  10. Keim C. N., Farina M., Lins U. ( 2007a). Magnetoglobus, magnetic aggregates in anaerobic environments. Microbe 2:437–445
    [Google Scholar]
  11. Keim C. N., Martins J. L., de Barros H. L., Lins U., Farina M. ( 2007b). Structure, behavior, ecology and diversity of multicellular magnetotactic prokaryotes. Magnetoreception and Magnetosomes in Bacteria103–132 Schüler D. Berlin: Springer; [View Article]
    [Google Scholar]
  12. Komeili A. ( 2012). Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiol Rev 36:232–255 [View Article][PubMed]
    [Google Scholar]
  13. Lane D. J. ( 1991). 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics115–175 Stackebrandt E. , Goodfellow M. Chichester: Wiley;
    [Google Scholar]
  14. Lefèvre C. T., Bazylinski D. A. ( 2013). Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev 77:497–526 [View Article][PubMed]
    [Google Scholar]
  15. Lefèvre C. T., Wu L. F. ( 2013). Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol 21:534–543 [View Article][PubMed]
    [Google Scholar]
  16. Lefèvre C. T., Santini C. L., Bernadac A., Zhang W. J., Li Y., Wu L. F. ( 2010). Calcium ion-mediated assembly and function of glycosylated flagellar sheath of marine magnetotactic bacterium. Mol Microbiol 78:1304–1312 [View Article][PubMed]
    [Google Scholar]
  17. Lefèvre C. T., Viloria N., Schmidt M. L., Pósfai M., Frankel R. B., Bazylinski D. A. ( 2012). Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J 6:440–450 [View Article][PubMed]
    [Google Scholar]
  18. Lin W., Li J., Pan Y. ( 2012). Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl Environ Microbiol 78:668–675 [View Article][PubMed]
    [Google Scholar]
  19. Lin W., Bazylinski D. A., Xiao T., Wu L. F., Pan Y. ( 2013). Life with compass: diversity and biogeography of magnetotactic bacteria. Environ Microbiol [View Article][PubMed]
    [Google Scholar]
  20. Lins U., Farina M. ( 1999). Phosphorus-rich granules in uncultured magnetotactic bacteria. FEMS Microbiol Lett 172:23–28 [View Article]
    [Google Scholar]
  21. Manz W., Amann R., Ludwig W., Wagner M., Schleifer K. H. ( 1992). Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600 [View Article]
    [Google Scholar]
  22. Otsuka Y., Muramatsu Y., Nakagawa Y., Matsuda M., Nakamura M., Murata H. ( 2011). Burkholderia oxyphila sp. nov., a bacterium isolated from acidic forest soil that catabolizes (+)-catechin and its putative aromatic derivatives. Int J Syst Evol Microbiol 61:249–254 [View Article][PubMed]
    [Google Scholar]
  23. Pernthaler A., Pernthaler J., Amann R. ( 2002). Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101 [View Article][PubMed]
    [Google Scholar]
  24. Pósfai M., Lefèvre C. T., Trubitsyn D., Bazylinski D. A., Frankel R. B. ( 2013). Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front Microbiol 4:344 [View Article][PubMed]
    [Google Scholar]
  25. Rodgers F. G., Blakemore R. P., Blakemore N. A., Frankel R. B., Bazylinski D. A., Maratea D., Rodgers C. ( 1990). Intercellular structure in a many-celled magnetotactic prokaryote. Arch Microbiol 154:18–22 [View Article]
    [Google Scholar]
  26. Saitou N., Nei M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  27. Simmons S. L., Bazylinski D. A., Edwards K. J. ( 2007). Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ Microbiol 9:2162–2174 [View Article][PubMed]
    [Google Scholar]
  28. Spring S., Bazylinski D. A. ( 2006). Magnetotactic bacteria. The Prokaryotes842–862 Dworkin M., Falkow S., Rosenberg E., Schleifer K.-H., Stackebrandt E. . New York: Springer; [View Article]
    [Google Scholar]
  29. Spring S., Amann R., Ludwig W., Schleifer K. H., van Gemerden H., Petersen N. ( 1993). Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microbiol 59:2397–2403[PubMed]
    [Google Scholar]
  30. Tamura K., Dudley J., Nei M., Kumar S. ( 2007). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  31. Thompson J. D., Higgins D. G., Gibson T. J. ( 1994). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  32. Wang Y., Lin W., Li J., Pan Y. ( 2013). High diversity of magnetotactic Deltaproteobacteria in a freshwater niche. Appl Environ Microbiol 79:2813–2817 [View Article][PubMed]
    [Google Scholar]
  33. Wolfe R. S., Thauer R. K., Pfennig N. A. ( 1987). A “capillary racetrack” method for isolation of magnetotactic bacteria. FEMS Microbiol Ecol 45:31–35 [View Article]
    [Google Scholar]
  34. Zhang W. Y., Zhou K., Pan H. M., Du H. J., Chen Y. R., Zhang R., Ye W., Lu C., Xiao T., Wu L. F. ( 2013). Novel rod-shaped magnetotactic bacteria belonging to the class Alphaproteobacteria. Appl Environ Microbiol 79:3137–3140 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.078717-0
Loading
/content/journal/micro/10.1099/mic.0.078717-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error