Dataset Information

Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum.

ABSTRACT: Magnetotactic bacteria (MTB) are known to produce single-domain magnetite or greigite crystals within intracellular membrane organelles and to navigate along the Earth's magnetic field lines. MTB have been suggested as being one of the most ancient biomineralizing metabolisms on the Earth and they represent a fundamental model of intracellular biomineralization. Moreover, the determination of their specific crystallographic signature (e.g. structure and morphology) is essential for palaeoenvironmental and ancient-life studies. Yet, the mechanisms of MTB biomineralization remain poorly understood, although this process has been extensively studied in several cultured MTB strains in the Proteobacteria phylum. Here, we show a comprehensive transmission electron microscopy (TEM) study of magnetic and structural properties down to atomic scales on bullet-shaped magnetites produced by the uncultured strain MYR-1 belonging to the Nitrospirae phylum, a deeply branching phylogenetic MTB group. We observed a multiple-step crystal growth of MYR-1 magnetite: initial isotropic growth forming cubo-octahedral particles (less than approx. 40 nm), subsequent anisotropic growth and a systematic final elongation along [001] direction. During the crystal growth, one major {111} face is well developed and preserved at the larger basal end of the crystal. The basal {111} face appears to be terminated by a tetrahedral-octahedral-mixed iron surface, suggesting dimensional advantages for binding protein(s), which may template the crystallization of magnetite. This study offers new insights for understanding magnetite biomineralization within the Nitrospirae phylum.

SUBMITTER: Li J

PROVIDER: S-EPMC4305428 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum.

Li Jinhua J Menguy Nicolas N Gatel Christophe C Boureau Victor V Snoeck Etienne E Patriarche Gilles G Leroy Eric E Pan Yongxin Y

Journal of the Royal Society, Interface 20150201 103

Magnetotactic bacteria (MTB) are known to produce single-domain magnetite or greigite crystals within intracellular membrane organelles and to navigate along the Earth's magnetic field lines. MTB have been suggested as being one of the most ancient biomineralizing metabolisms on the Earth and they represent a fundamental model of intracellular biomineralization. Moreover, the determination of their specific crystallographic signature (e.g. structure and morphology) is essential for palaeoenviron ...[more]

PMID: 25566884

Similar Datasets

Project description:Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that form intracellular nanoparticles of magnetite (Fe3O4) or greigite (Fe3S4) in a genetically controlled manner. Magnetite and greigite synthesis requires MTB to transport a large amount of iron from the environment. Most intracellular iron was proposed to be contained within the crystals. However, recent mass spectrometry studies suggest that MTB may contain a large amount of iron that is not precipitated in crystals. Here, we attempted to resolve these discrepancies by performing chemical and magnetic assays to quantify the different iron pools in the magnetite-forming strain Magnetospirillum magneticum AMB-1, as well as in mutant strains showing defects in crystal precipitation, cultivated at various iron concentrations. All results show that magnetite represents at most 30% of the total intracellular iron under our experimental conditions and even less in the mutant strains. We further examined the iron speciation and subcellular localization in AMB-1 using the fluorescent indicator FIP-1, which was designed for the detection of labile Fe(II). Staining with this probe suggests that unmineralized reduced iron is found in the cytoplasm and associated with magnetosomes. Our results demonstrate that, under our experimental conditions, AMB-1 is able to accumulate a large pool of iron distinct from magnetite. Finally, we discuss the biochemical and geochemical implications of these results.IMPORTANCE Magnetotactic bacteria (MTB) produce iron-based intracellular magnetic crystals. They represent a model system for studying iron homeostasis and biomineralization in microorganisms. MTB sequester a large amount of iron in their crystals and have thus been proposed to significantly impact the iron biogeochemical cycle. Several studies proposed that MTB could also accumulate iron in a reservoir distinct from their crystals. Here, we present a chemical and magnetic methodology for quantifying the iron pools in the magnetotactic strain AMB-1. Results showed that most iron is not contained in crystals. We then adapted protocols for the fluorescent Fe(II) detection in bacteria and showed that iron could be detected outside crystals using fluorescence assays. This work suggests a more complex picture for iron homeostasis in MTB than previously thought. Because iron speciation controls its fate in the environment, our results also provide important insights into the geochemical impact of MTB.

Project description:Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (Fe3O4), and/or greigite (Fe3S4) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the Nitrospirae phylum can form up to several hundreds of Fe3O4 magnetosome crystals and dozens of sulfur globules in a single cell. These MTB are widespread in aquatic environments and sometimes account for a significant proportion of microbial biomass near the oxycline, linking these lineages to the key steps of global iron and sulfur cycling. Despite their ecological and biogeochemical importance, our understanding of the diversity and ecophysiology of magnetotactic Nitrospirae is still very limited because this group of MTB remains unculturable. Here, we identify and characterize two previously unknown MTB populations within the Nitrospirae phylum through a combination of 16S rRNA gene-based and genome-resolved metagenomic analyses. These two MTB populations represent distinct morphotypes (rod-shaped and coccoid, designated as XYR, and XYC, respectively), and both form more than 100 bullet-shaped magnetosomal crystals per cell. High-quality draft genomes of XYR and XYC have been reconstructed, and they represent a novel species and a novel genus, respectively, according to their average amino-acid identity values with respect to available genomes. Accordingly, the names Candidatus Magnetobacterium cryptolimnobacter and Candidatus Magnetomicrobium cryptolimnococcus for XYR and XYC, respectively, were proposed. Further comparative genomic analyses of XYR, XYC, and previously reported magnetotactic Nitrospirae reveal the general metabolic potential of this MTB group in distinct microenvironments, including CO2 fixation, dissimilatory sulfate reduction, sulfide oxidation, nitrogen fixation, or denitrification processes. A remarkably conserved magnetosome gene cluster has been identified across Nitrospirae MTB genomes, indicating its putative important adaptive roles in these bacteria. Taken together, the present study provides novel insights into the phylogenomic diversity and ecophysiology of this intriguing, yet poorly understood MTB group.

Dataset Information

Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum.

Publications

Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets