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

Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12263-8. doi: 10.1073/pnas.1001290107. Epub 2010 Jun 21.

Abstract

Intracellular magnetite crystal formation by magnetotactic bacteria has emerged as a powerful model for investigating the cellular and molecular mechanisms of biomineralization, a process common to all branches of life. Although magnetotactic bacteria are phylogenetically diverse and their crystals morphologically diverse, studies to date have focused on a few, closely related species with similar crystal habits. Here, we investigate the process of magnetite biomineralization in Desulfovibrio magneticus sp. RS-1, the only reported species of cultured magnetotactic bacteria that is outside of the alpha-Proteobacteria and that forms bullet-shaped crystals. Using a variety of high-resolution imaging and analytical tools, we show that RS-1 cells form amorphous, noncrystalline granules containing iron and phosphorus before forming magnetite crystals. Using NanoSIMS (dynamic secondary ion mass spectroscopy), we show that the iron-phosphorus granules and the magnetite crystals are likely formed through separate cellular processes. Analysis of the cellular ultrastructure of RS-1 using cryo-ultramicrotomy, cryo-electron tomography, and tomography of ultrathin sections reveals that the magnetite crystals are not surrounded by membranes but that the iron-phosphorus granules are surrounded by membranous compartments. The varied cellular paths for the formation of these two minerals lead us to suggest that the iron-phosphorus granules constitute a distinct bacterial organelle.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cryoelectron Microscopy
  • Crystallization
  • Cytoplasmic Granules / chemistry
  • Cytoplasmic Granules / metabolism*
  • Desulfovibrio / chemistry
  • Desulfovibrio / metabolism*
  • Desulfovibrio / ultrastructure
  • Electron Microscope Tomography
  • Ferrosoferric Oxide / chemistry
  • Iron / metabolism*
  • Magnetosomes / metabolism
  • Magnetosomes / ultrastructure
  • Microscopy, Electron, Transmission
  • Minerals / chemistry
  • Periplasm / metabolism
  • Periplasm / ultrastructure
  • Phosphorus / metabolism*

Substances

  • Minerals
  • Phosphorus
  • Iron
  • Ferrosoferric Oxide