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

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.

Magnetotactic Bacteria Accumulate a Large Pool of Iron Distinct from Their Magnetite Crystals

“…It is unclear whether this Fe(II) would be contained inside magnetosomes, within the magnetosome membrane, or at the magnetosome surface. From high-resolution electron microscope analyses, Werckmann and collaborators proposed that iron could accumulate in the magnetosome membrane before its precipitation as magnetite ( 38 ). Our observations are in line with these results and indicate that iron in the magnetosome membrane would at least be composed of Fe(II) species.…”

Iron‐biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples

“…Alternatively, ferrous iron could be transported to mature magnetosome vesicles across the magnetosome membrane. The latter hypothesis was recently supported by two high‐resolution electron microscopy and fluorescence studies, which evidenced a layer of unmineralized ferrous ions surrounding magnetite in the magnetosome membrane in both cultured and environmental bacteria (Werckmann et al ., 2017; Amor et al ., 2020b). In that regard, genes encoding Fe(II) transporters ( feoAB operon) have been found in the vicinity of all MCGs of MTB with their genome sequenced (Suzuki et al ., 2006; Rong et al ., 2008, 2012; Uebe and Schüler, 2016).…”

Isolation of Magnetotactic Bacteria From Environmental Samples and Optimization and Characterization of Extracted Magnetosomes

“…In MTB, the magnetosome biomineralization process is under genetic and biochemical control. Specific genes are involved in the biomineralization and production of the magnetosome crystals (Werckmann et al, 2017).…”