Transformation Cycle of Magnetosomes in Human Stem Cells: From Degradation to Biosynthesis of Magnetic Nanoparticles Anew

The nanoparticles produced by magnetotactic bacteria, called magnetosomes, are made of a magnetite core with high levels of crystallinity surrounded by a lipid bilayer. This organized structure has been developed during the course of evolution of these organisms to adapt to their specific habitat an...

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Published inACS nano Vol. 14; no. 2; pp. 1406 - 1417
Main Authors Curcio, Alberto, Van de Walle, Aurore, Serrano, Aida, Preveral, Sandra, Péchoux, Christine, Pignol, David, Menguy, Nicolas, Lefevre, Christopher T, Espinosa, Ana, Wilhelm, Claire
Format Journal Article
LanguageEnglish
Published United States American Chemical Society 25.02.2020
Subjects
Biotechnology
Cells, Cultured
Humans
Life Sciences
Magnetite Nanoparticles - chemistry
Magnetosomes - chemistry
Magnetosomes - metabolism
Mesenchymal Stem Cells - chemistry
Mesenchymal Stem Cells - metabolism
Particle Size
Surface Properties
magnetosomes
magnetite
biodegradation
nanoparticles
ferrihydrite
biosynthesis
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Summary:The nanoparticles produced by magnetotactic bacteria, called magnetosomes, are made of a magnetite core with high levels of crystallinity surrounded by a lipid bilayer. This organized structure has been developed during the course of evolution of these organisms to adapt to their specific habitat and is assumed to resist degradation and to be able to withstand the demanding biological environment. Herein, we investigated magnetosomes’ structural fate upon internalization in human stem cells using magnetic and photothermal measurements, electron microscopy, and X-ray absorption spectroscopy. All measurements first converge to the demonstration that intracellular magnetosomes can experience an important biodegradation, with up to 70% of their initial content degraded, which is associated with the progressive storage of the released iron in the ferritin protein. It correlates with an extensive magnetite to ferrihydrite phase transition. The ionic species delivered by this degradation could then be used by the cells to biosynthesize magnetic nanoparticles anew. In this case, cell magnetism first decreased with magnetosomes being dissolved, but then cells remagnetized entirely, evidencing the neo-synthesis of biogenic magnetic nanoparticles. Bacteria-made biogenic magnetosomes can thus be totally remodeled by human stem cells, into human cells-made magnetic nanoparticles.
ISSN:1936-0851
1936-086X
DOI:10.1021/acsnano.9b08061