Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates

Abstract

The iron oxide mineral magnetite (Fe 3 O 4 ) is produced by various organisms to exploit magnetic and mechanical properties. Magnetotactic bacteria have become one of the best model organisms for studying magnetite biomineralization, as their genomes are sequenced and tools are available for their genetic manipulation. However, the chemical route by which magnetite is formed intracellularly within the so-called magnetosomes has remained a matter of debate. Here we used X-ray absorption spectroscopy at cryogenic temperatures and transmission electron microscopic imaging techniques to chemically characterize and spatially resolve the mechanism of biomineralization in those microorganisms. We show that magnetite forms through phase transformation from a highly disordered phosphate-rich ferric hydroxide phase, consistent with prokaryotic ferritins, via transient nanometric ferric (oxyhydr)oxide intermediates within the magnetosome organelle. This pathway remarkably resembles recent results on synthetic magnetite formation and bears a high similarity to suggested mineralization mechanisms in higher organisms.ferrihydrite | geomagnetism | hematite | nanoparticles | precursors

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

“…In contrast, excision of mamI in M. gryphiswaldense did not entirely abolish the biomineralization of electron-dense iron-rich particles, but the mutant still synthesized tiny and poorly crystalline nonmagnetic particles, which in some cases were shown to consist of hematite. Recent findings for M. gryphiswaldense and M. magneticum indicate that the observed poorly ordered iron (oxyhydr)oxide phases are precursors to the magnetite phase in bacteria (41,52). In addition, the ability of MamP to precipitate ferrihydrite and magnetite in vitro suggests that magnetite may be formed through a stepwise phase transformation process (48).…”

Correlative Electron and Fluorescence Microscopy of Magnetotactic Bacteria in Liquid: Toward In Vivo Imaging

“…Materials characterization techniques are typically aimed at direct observations of the magnetite nucleation and growth at high spatial resolution. High resolution TEM is often used to observe formation of magnetosomes in magnetotactic bacteria via cryogenic TEM (cryo-TEM) 4 …”

“…Biomineralization of inorganic materials in single cell organisms is an ideal system for studying fundamental mechanisms of biomineralization 1 . Model systems range from prokaryotic organisms, such as magnetite formation in magnetotactic bacteria [2][3][4] , to eukaryotic organisms, such as silica biomineralization in diatoms 5,6 . Understanding biomineralization in these organisms in terms of crystal nucleation and growth, as well as the involvement of biological macromolecules and cellular processes, is of fundamental interest to scientists as similar principles can be used to develop synthetic nanomaterials.…”

“…Materials characterization techniques are typically aimed at direct observations of the magnetite nucleation and growth at high spatial resolution. High resolution TEM is often used to observe formation of magnetosomes in magnetotactic bacteria via cryogenic TEM (cryo-TEM) 4,[22][23][24][25][26][27][28][29] . This technique provides vital information about organization of the cellular structures and development of the magnetosomes 20,27 .…”

Biosynthesis of Nanoparticles from Halophiles

“…Interactions between metals and microbes are well documented and have been exploited for various applications in the fi elds of biomineralization, bioleaching and bioremediation (Klaus-Joerger et al 2001 ). Many magnetotactic bacteria are known to naturally produce nanostructured mineral crystals that have properties similar to chemically synthesized materials (Baumgartner et al 2013 ). Such nano-factories exercise strict control over size, shape and composition through compartmentalization in the periplasmic space and vesicles.…”