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 α-Proteobacteria and that forms bulletshaped 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.bacterial organelle | biomineralization | magnetotactic bacteria | dynamic secondary ion mass spectroscopy | magnetite B iomineralization, the biologically controlled transformation of inorganic compounds into highly-ordered structures, is performed by organisms in all branches of life, from bacteria to humans. Because biogenic minerals often have superior properties to their chemically synthesized counterparts, understanding biomineralization is important to fields as diverse as inorganic materials synthesis and medicine (1, 2). Among the numerous organisms capable of biomineralization, magnetotactic bacteria (MB), a group of microbes that form intracellular chains of magnetic minerals including magnetite and greigite, have become powerful models for studying biomineralization because of their relatively fast growth rate and genetic tractability (3).Investigation of the cellular ultrastructure of MB has shown that the magnetite crystals are formed within membranous intracellular compartments called magnetosomes, which are present before the formation of magnetite (4, 5). Other studies have shown that when magnetite formation is induced by decreasing oxygen levels or adding iron to iron-deprived cells, multiple crystals in the chain nucleate simultaneously (5, 6). These insights into the kinetics of magnetite biomineralization have been complemented by molecular studies. A genomic island called the magnetosome island (MAI) has been found in all MB studied to date. Loss of the MAI results in an absence of magnetosome membranes and magnetite crystals, and gene...

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

“…This led to speculations that bulletshaped magnetosomes are generally not formed within a MM, and that these MTB may have evolved a divergent molecular mechanism of magnetite biomineralization (13,14). However, our discovery of similar structures and genes in this study is strongly indicative of homologous mechanisms of biomineralization also in distantly related MTB outside the Proteobacteria.…”

“…Because previous studies failed to detect a membrane around magnetosomes of Mbav, it was speculated that non-α MTB producing bullet-shaped magnetite crystals might use different biomineralization mechanisms based on "templates" that might be fundamentally divergent from the MM-dependent mechanism in magnetospirilla and related MTB (13,14).…”

“…The presence of MTB within unrelated lines of various phylogenetic groups, as well as their stunning diversity with respect to magnetosome shape, composition, and intracellular organization lead to speculations of whether the evolutionary origin of magnetotaxis is polyphyletic. Thus, independent origins and subsequent convergent evolution were proposed for greigite and magnetite producing MTB (12), and it has been suggested that those MTB forming magnetic crystals of divergent shapes or composition may use different mechanisms of magnetosome formation (13,14).…”

Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria

“…M. multicellularis is similar but these microorganisms appear to be distinct in the presence/absence of a membrane enveloping the crystals and in their magnetosome crystal morphologies. The absence of a magnetosome membrane in D. magneticus (Byrne et al, 2010) may explain the irregular morphologies of magnetite formed by this microorganism despite the presence of mam genes in its genome (Nakazawa et al, 2009). Ca.…”

Characterization of uncultured giant rod-shaped magnetotactic Gammaproteobacteria from a freshwater pond in Kanazawa, Japan

“…These magnetosomes function as a cellular magnetic compass in magnetotaxis motility that is directed along the geomagnetic field or in an applied magnetic field. Other intracellular structures that have been found in MTB are inclusions composed of elements such as phosphorus (Lins & Farina, 1999), iron-phosphorus (Byrne et al, 2010), sulfur (Keim et al, 2005), calcium (Isambert et al, 2007) or polyhydroxybutyrate (Gorby et al, 1988). Because of their involvement with these various ions, MTB probably play a significant role in geochemical cycling (Simmons et al, 2007).…”