Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes.
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.
Byrne
Meghan E
ME
Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA.
Ball
David A
DA
Guerquin-Kern
Jean-Luc
JL
Rouiller
Isabelle
I
Wu
Ting-Di
TD
Downing
Kenneth H
KH
Vali
Hojatollah
H
Komeili
Arash
A
D020285:Cryoelectron Microscopy; D003460:Crystallization; D003594:Cytoplasmic Granules / Q000737:chemistry / Q000378:metabolism*; D003901:Desulfovibrio / Q000737:chemistry / Q000378:metabolism* / Q000648:ultrastructure; D055032:Electron Microscope Tomography; D052203:Ferrosoferric Oxide / Q000737:chemistry; D007501:Iron / Q000378:metabolism*; D055944:Magnetosomes / Q000378:metabolism / Q000648:ultrastructure; D046529:Microscopy, Electron, Transmission; D008903:Minerals / Q000737:chemistry; D019897:Periplasm / Q000378:metabolism / Q000648:ultrastructure; D010758:Phosphorus / Q000378:metabolism*
D008903:Minerals; D010758:Phosphorus; D007501:Iron; D052203:Ferrosoferric Oxide