title: Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes.
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.
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA.
authors.forename: Meghan E
authors.initials: ME
authors.lastname: Byrne
authors.forename: David A
authors.initials: DA
authors.lastname: Ball
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Guerquin-Kern
authors.forename: Isabelle
authors.initials: I
authors.lastname: Rouiller
authors.forename: Ting-Di
authors.initials: TD
authors.lastname: Wu
authors.forename: Kenneth H
authors.initials: KH
authors.lastname: Downing
authors.forename: Hojatollah
authors.initials: H
authors.lastname: Vali
authors.forename: Arash
authors.initials: A
authors.lastname: Komeili
mesh_terms: 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*
chemical_list: D008903:Minerals; D010758:Phosphorus; D007501:Iron; D052203:Ferrosoferric Oxide