Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of theNitrospiraephylum

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 f111g face is well developed and preserved at the larger basal end of the crystal. The basal f111g 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.

Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes

“…However, traditional optical and fluorescence microscopy cannot detect the structural features of magnetosomes due to their limitation in spatial resolution at around 0.2 μm. In the past decades TEM has made significant progress on both spatial and energy resolution, and now provides a powerful platform for obtaining simultaneous structural, compositional, and magnetic characterization of a single MTB cell down to the atomic scale (Pósfai et al, 2013b; Li and Pan, 2015; Li et al, 2015). On the other hand, TEM cannot provide phylogenetic affiliation information on the bacteria.…”

Phylogenetic and Structural Identification of a Novel MagnetotacticDeltaproteobacteriaStrain, WYHR-1, from a Freshwater Lake

“…From high-resolution TEM (HRTEM) observations it can be seen that mature WYHR-1 magnetosomes are straight and elongated along the [001] direction and have a bullet-shaped morphology with a large flat end terminated by a {100} face at the base and a conical top. This crystal morphology is distinctively different from bullet-shaped magnetosomes produced by other magnetotactic Deltaproteobacteria and Nitrospirae (30,31,(33)(34)(35). This indicates that, consistent with its novel taxonomic status, WYHR-1 may also have a different crystal growth process and mechanism that results from species-specific magnetosome biomineralization in MTB.…”

“…The method generally consists of four steps: (i) enrichment of MTB cells from an environmental sample, (ii) 16S rRNA gene sequencing of MTB, and (iii) fluorescence in situ hybridization (FISH) analyses coordinated with (iv) transmission electron microscope (TEM) or scanning electron microscope (SEM) observations of the probe-hybridized cells (29). Once the MTB is identified phylogenetically and structurally through this so-called coupled FISH-SEM or FISH-TEM approach, we characterize the mineralogy, crystallography, and magnetism of magnetosomes formed by these uncultured MTB as illustrated recently, e.g., by combined magnetic and advanced TEM analyses from micrometer to atomic scales (30,32).…”

“…Although phylogenetic diversity has been well assessed, detailed morphological and mineralogical studies of diverse MTB remain sparse (28)(29)(30)(31). The challenge is that these strains are extremely difficult to culture, and the chemical and crystallographic properties of their magnetosomes must therefore be characterized within complex populations of diverse microbes in environmental samples.…”

Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum

“…Intracellular sulphur globules were also detected in Nitrospirae magnetotactic bacteria Ca . Magnetobacterium bavaricum, LO‐1, MWB‐1 and MYR‐1 (Jogler et al, ; Li et al, ; Lefevre et al, ; Lin et al, ; Li et al, ), and those in the Ca . Magnetobacterium bavarium are present in the form of cyclo‐octa sulphur (S8) (Eder et al, ).…”