Probing the nanostructure and arrangement of bacterial magnetosomes by small-angle x-ray scattering

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Rosenfeldt, Sabine ; Riese, Cornelius N. ; Mickoleit, Frank ; Schüler, Dirk ; Schenk, Anna:
Probing the nanostructure and arrangement of bacterial magnetosomes by small-angle x-ray scattering.
In: Applied and Environmental Microbiology. Bd. 85 (2019) Heft 24 . - e01513-19.
ISSN 1098-5336
DOI: https://doi.org/10.1128/AEM.01513-19

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Abstract

Magnetosomes are membrane-enveloped single-domain ferromagnetic nanoparticles enabling the navigation of magnetotactic bacteria along magnetic field lines. Strict control over each step of biomineralization generates particles of high crystallinity, strong magnetization and remarkable uniformity in size and shape, particularly interesting for many biomedical and biotechnological applications. However, to understand the physicochemical processes involved in magnetite biomineralization, precise and permanent monitoring of particle production is required. Common techniques such as transmission electron microscopy (TEM) or Fe measurements only allow for semi-quantitative assessment of the magnetosome formation without routinely revealing quantitative structural information. In this study, lab-based small-angle x-ray scattering (SAXS) is explored as a means to monitor the different stages of magnetosome biogenesis in the model organism Magnetospirillum gryphiswaldense. SAXS is evaluated as a quantitative stand-alone technique to analyse the size, shape and arrangement of magnetosomes in cells cultivated under different growth conditions. By applying a simple and robust fitting procedure based on linearly aligned spheres, it is demonstrated that the SAXS datasets contain information on both the diameter of the inorganic crystal and the protein-rich magnetosome membrane. The analyses reveal a narrow particle size distribution with an overall magnetosome radius of 19 nm in Magnetospirillum gryphiswaldense. Furthermore, the averaged distance between individual magnetosomes is determined, revealing a chain-like particle arrangement with a center-to-center distance of 53 nm. Overall, these data demonstrate that SAXS can be used as a novel stand-alone technique allowing for the at-line monitoring of magnetosome biosynthesis, thereby providing accurate information on the particle nanostructure.Importance This study explores lab-based small-angle x-ray scattering (SAXS) as a novel quantitative stand-alone technique to monitor the size, shape and arrangement of magnetosomes during different stages of particle biogenesis in the model organism Magnetospirillum gryphiswaldense. The SAXS datasets contain volume-averaged, statistically accurate information on both the diameter of the inorganic nanocrystal and the enveloping protein-rich magnetosome membrane. As a robust and non-destructive in-situ technique, SAXS can provide new insights into the physicochemical steps involved in the biosynthesis of magnetosome nanoparticles as well as their assembly into well-ordered chains. The proposed fit model can be easily adapted to account for different particle shapes and arrangements produced by other strains of magnetotactic bacteria, thus rendering SAXS a highly versatile method.