Archives of Microbiology

, Volume 160, Issue 1, pp 35–42 | Cite as

Copper association with iron sulfide magnetosomes in a magnetotactic bacterium

  • Dennis A. Bazylinski
  • Anthony J. Garratt-Reed
  • Afshin Abedi
  • Richard B. Frankel
Original Papers


Greigite (Fe3S4) and pyrite (FeS2) particles in the magnetosomes of a many-celled, magnetotactic prokaryote (MMP), common in brackish-to-marine, sulfidic, aquatic habitats, contained relatively high concentrations of copper which ranged from about 0.1 to 10 atomic per cent relative to iron. In contrast, the greigite particles in the magnetosomes of a curved magnetotactic bacterium collected from the same sampling site did not contain significant levels of copper. The ability of the MMP to biomineralize copper within its magnetosomes appeared to be limited to that organism and dependent upon the site from which it was collected. Although the chemical mechanism and physiological function of copper accumulation in the magnetosomes of the MMP is unclear, the presence of copper is the first evidence that another transition metal ion could be incorporated in the mineral phase of the magnetosomes of a magnetotactic bacterium.

Key words

Biomineralization Copper concentration Greigite Iron sulfide Magnetite Magnetosome Magnetotactic bacterium Pyrite Single magneticdomain 



many-celled magnetotactic prokaryote


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Balkwill DL, Maratea D, Blakemore RP (1980) Ultrastructure of a magnetotactic spirillum. J Bacteriol 141: 1399–1408Google Scholar
  2. Bazylinski DA (1991) Bacterial production of iron sulfides. In: Alpert M, Calvert P, Frankel RB, Rieke P, Tirrell D (eds) Materials syntheses based on biological processes. Materials Research Society, Pittsburg, Pa., pp 81–91Google Scholar
  3. Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic magnetite production by a marine magnetotactic bacterium. Nature 334: 518–519Google Scholar
  4. Bazylinski DA, Frankel RB, Garratt-Reed AJ, Mann S (1990) Biomineralization of iron sulfides in magnetotactic bacteria from sulfidic environments. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum Press, New York, pp 239–255Google Scholar
  5. Bazylinski DA, Garratt-Reed AJ, Frankel RB (1993) Electron microscopic studies of magnetosomes in magnetotactic bacteria. J Electron Microsc Tech (in press)Google Scholar
  6. Bender CL, Cooksey DA (1986) Indigenous plasmids in Pseudomonas syringae py. tomato: conjugative transfer and role in copper resistance. J Bacteriol 165: 534–541Google Scholar
  7. Bender CL, Cooksey DA (1987) Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato J Bacteriol 169: 470–474Google Scholar
  8. Blakemore RP (1975) Magnetotactic bacteria. Science 190: 377–379Google Scholar
  9. Blakemore RP (1982) Magnetotactic bacteria. Annu Rev Microbiol 36: 217–238Google Scholar
  10. Blakemore RP, Blakemore NA, Bazylinski DA, Moench TT (1989) Magnetotactic bacteria. In: Staley JT, Bryant EP, Pfennig N, Holt JG (eds) Bergey's manual of systematic bacteriology, vol 3. Williams & Wilkins, Baltimore, pp 1882–1888Google Scholar
  11. Canfield DE, Berner RA (1987) Dissolution and pyritization of magnetite in anoxic marine sediments. Geochim Cosmochim Acta 51: 645–659Google Scholar
  12. DeLong EF, Frankel RB, Bazylinski DA (1993) Multiple evolutionary origins of magnetotaxis in bacteria. Science 259: 803–806Google Scholar
  13. Erardi FX, Failla ML, Falkinham JOIII (1987) Plasmid-encoded copper resistance and percipitation by Mycobacterium scrofulaceum. Appl Environ Microbiol 53: 1951–1954Google Scholar
  14. Farina M, Lins de Barros HGP, Motta de Esqivel D, Danon J (1983) Ultrastructural of magnetotactic microorganism. Biol Cell 48: 85–88Google Scholar
  15. Farina M, Motta de Esqivel D, Lins de Barros HGP (1990) Magnetic iron-sulphur crystals from a magnetotactic microorganism. Nature 343: 256–258Google Scholar
  16. Frankel RB (1984) Magnetic guidance of organisms. Annu Rev Biophys Bioeng 13: 85–103Google Scholar
  17. Frankel RB, Bazylinski DA (1993) Structure and function of magnetosomes in magnetotactic bacteria. In: Aksay IA, Sarikaya M (eds) Design and processing of materials by biomimikking. American Institute of Physics, New York (in press)Google Scholar
  18. Frankel RB, Blakemore RP (1980) Navigational compass in magnetic bacteria. J Mag Mag Mat 15–18: 1562–1564Google Scholar
  19. Frankel RB, Blakemore RP (1989) Magnetite and magnetotaxis in microorganisms. Bioelectromagnetics 10: 223–237Google Scholar
  20. Frankel RB, Blakemore RP, Wolfe RS (1979) Magnetite in freshwater magnetotactic bacteria. Science 203: 1355–1356Google Scholar
  21. Gorby YA (1989) Regulation of magnetosome biogenesis by oxygen and nitrogen. Doctoral thesis, Department of Microbiology, University of New Hampshire, Durham, New HampshireGoogle Scholar
  22. Gorby YA, Beveridge TJ, Blakemore RP (1988) Characterization of the bacterial magnetosome membrane. J Bacteriol 170: 834–841Google Scholar
  23. Heywood BR, Bazylinski DA, Garratt-Reed AJ, Mann S, Frankel RB (1990) Controlled biosynthesis of greigite (Fe3S4) in magnetotactic bacteria. Naturwissenschaften 77: 536–538Google Scholar
  24. Heywood BR, Mann S, Frankel RB (1991) Structure, morphology, and growth of biogenic greigite (Fe3S4). In: Alpert M, Calvert P, Frankel RB, Rieke P, Tirrell D (eds) Materials syntheses based on biological processes. Materials Research Society, Pittsburg, Pa, pp 93–108Google Scholar
  25. Hirsch PB, Howie A, Nicholson B, Pashley DW, Whelan MJ (1977) Electron microscopy of thin crystals. Krieger, Huntington, NY, p 125Google Scholar
  26. Jones HE, Trudinger PA, Chambers LA, Pyliotis NA (1976) Metal accumulation by bacteria with particular reference to dissimilatory sulphate-reducing bacteria. Z Allg Mikrobiol 16: 425–435Google Scholar
  27. Kluckhohn RS (1990) Trace metals and pyrite in sediments of Chesapeake Bay. Master of Science Thesis, Department of Oceanography Old Dominion University, Norfolk, Va., pp 28–61Google Scholar
  28. Kobayashi K, Nomura M (1972) Iron sulfides in the sediment cores from the Sea of Japan and their geophysical implications. Earth Planet Sci Lett 16: 200–208Google Scholar
  29. Kostov I, Minceva-Stefanova J (1981) Sulphide minerals. Bulgarian Academy of Sciences, Sofia, p 212Google Scholar
  30. Lowenstam H (1981) Minerals formed by organisms. Science 211: 1126–1131Google Scholar
  31. Mann S (1986) On the nature of boundary-organized biomineralization. J Inorg Chem 28: 363–371Google Scholar
  32. Mann S, Frankel RB (1989) Magnetite biomineralization in unicellular microoganisms. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: chemical and biochemical perspectives. Verlag Chemie, Weinheim, pp 388–426Google Scholar
  33. Mann S, Sparks NHC, Blakemore RP (1987) Ultrastructure and characterization of anisotropic inclusions in magnetotactic bacteria. Proc R Soc Lond [Biol] 231: 477–487Google Scholar
  34. Mann S, Sparks NHC, Frankel RB, Bazylinski DA, Jannasch HW (1990) Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343: 258–260Google Scholar
  35. Matsuda T, Endo J, Osakabe N, Tonomura A, Arii T (1983) Morphology and structure of biogenic magnetite particles. Nature 302: 411–412Google Scholar
  36. Morse JW, Millero FJ, Cornwell JC, Rickard D (1987) The chemistry of the hydrogen sulfide and iron sulfide systems in natural waters. Earth-Sci Rev 24: 1–42Google Scholar
  37. Rheinheimer G (1992) Aquatic microbiology. Wiley, New York, p 134Google Scholar
  38. Rodgers FG, Blakemore RP, Blakemore NA, Frankel RB, Bazylinski DA, Maratea D, Rodgers C (1990a) Intercellular structure in a many-celled magnetotactic prokaryote. Arch Microbiol 154: 18–22Google Scholar
  39. Rodgers FG, Blakemore RP, Blakemore NA, Frankel RB, Bazylinski DA, Maratea D, Rodgers C (1990b) Intercellular junctions, motility and magnetosome structure in a multicellular magnetotactic prokaryote. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum Press, New York, pp 231–237Google Scholar
  40. Schleifer KH, Schuler D, Spring S, Weizenegger M, Amann R, Ludwig W, Kohler M (1991) The genus Magnetospirillum gen. nov. Description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. System Appl Microbiol 14: 379–385Google Scholar
  41. Silver S, Misra TK (1988) Plasmid-mediated heavy metal resistance. Annu Rev Microbiol 42: 717–743Google Scholar
  42. Towe KM, Moench TT (1991) Electron-optical characterization of bacterial magnetite. Earth Planet Sci Lett 52: 213–220Google Scholar
  43. Wolfe RS, Thauer RK, Pfennig N (1987) A “capillary racetrack” method for isolation of magnetotactic bacteria FEMS Microbiol Ecol 45: 31–35Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Dennis A. Bazylinski
    • 1
  • Anthony J. Garratt-Reed
    • 2
  • Afshin Abedi
    • 3
  • Richard B. Frankel
    • 3
  1. 1.Department of Anaerobic MicrobiologyVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  2. 2.Center for Materials ResearchMassachusetts Institute of TechnologyCambridgeUSA
  3. 3.Department of PhysicsCalifornia Polytechnic State UniversitySan Luis ObispoUSA

Personalised recommendations