Localized iron accumulation precedes nucleation and growth of magnetite crystals in magnetotactic bacteria

Jacques Werckmann,Ulysses Lins,Ovidiu Ersen,Jefferson Cypriano,Marcos Farina,Dennis A Bazylinski,Kassiogé Dembelé,Christopher T Lefèvre

doi:10.1038/s41598-017-08994-9

Abstract

Many magnetotactic bacteria (MTB) biomineralize magnetite crystals that nucleate and grow inside intracellular membranous vesicles that originate from invaginations of the cytoplasmic membrane. The crystals together with their surrounding membranes are referred to magnetosomes. Magnetosome magnetite crystals nucleate and grow using iron transported inside the vesicle by specific proteins. Here we address the question: can iron transported inside MTB for the production of magnetite crystals be spatially mapped using electron microscopy? Cultured and uncultured MTB from brackish and freshwater lagoons were studied using analytical transmission electron microscopy in an attempt to answer this question. Scanning transmission electron microscopy was used at sub-nanometric resolution to determine the distribution of elements by implementing high sensitivity energy dispersive X-ray (EDS) mapping and electron energy loss spectroscopy (EELS). EDS mapping showed that magnetosomes are enmeshed in a magnetosomal matrix in which iron accumulates close to the magnetosome forming a continuous layer visually appearing as a corona. EELS, obtained at high spatial resolution, confirmed that iron was present close to and inside the lipid bilayer magnetosome membrane. This study provides important clues to magnetite formation in MTB through the discovery of a mechanism where iron ions accumulate prior to magnetite biomineralization.

Highlights

Over 60 different minerals are known to be produced by organisms in a process called biomineralization[1]
Imaging isolated magnetosomes from cultured bacteria and inside whole mounts of uncultured magnetotactic cocci was done with conventional transmission electron microscopy (CTEM), high resolution transmission electron microscopy (HRTEM), scanning transmission electron microscopy (STEM) and high angle annular dark-field (HAADF) to determine the best imaging conditions
The images obtained in HRTEM mode are phase contrast images

Summary

Introduction

Over 60 different minerals are known to be produced by organisms in a process called biomineralization[1]. One remarkable example of biomineralization is the synthesis of chains of nano-sized, membrane-bounded, iron-rich magnetic mineral crystals called magnetosomes by magnetotactic bacteria (MTB) These intracellular chains of organelles, either composed of magnetite (Fe3O4) or greigite (Fe3S4), impart to the cell a sufficiently large magnetic moment to allow for the passive alignment of the bacteria in the Earth’s geomagnetic field[3]. New and important results concerning the process of Fe3O4 biomineralization were obtained from 5 types of MTB These findings include: (1) Fe3O4 magnetosomes are surrounded by a matrix that seems to sequester significant amounts of Fe ions; and (2) Fe ions accumulate around all faces outside the magnetosome crystal and inside the lipid bilayer membrane of magnetosomes before their transfer to the forming crystal probably due to the actions of specific proteins. These findings together suggest that Fe migration and accumulation mechanisms precede nucleation and growth of Fe3O4 crystals in MTB

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