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Current view of iron biomineralization in magnetotactic bacteria

ABSTRACT: Graphical abstract Highlights • Iron biomineralization into magnetic nanoparticles by Magnetotactic bacteria (MTB).• Magnetosome formation mechanism presented in four main steps.• Magnetosome-associated proteins (MAPs) regulate the biomineralization process.• Chain arrangement and crystals morphology Variations exist between different MTB. Biomineralization is the process of mineral formation by living organisms. One notable example of these organisms is magnetotactic bacteria (MTB). MTB are Gram-negative bacteria that can biomineralize iron into magnetic nanoparticles. This ability allows these aquatic microorganisms to orient themselves according to the geomagnetic field. The biomineralization process takes place in a specialized sub-cellular membranous organelle, the magnetosome. The magnetosome contains a defined set of magnetosome-associated proteins (MAPs) that controls the biomineralization environment, including iron concentration, redox, and pH. Magnetite formation is subjected to a tight regulation within the magnetosome that affects the nanoparticle nucleation, size, and shape, leading to well-defined magnetic properties. The formed magnetite nanoparticles have unique characteristics of a stable, single magnetic domain with narrow size distribution and high crystalline structures, which turned MTB into the subject of interest in multidisciplinary research. This graphical review provides a current overview of iron biomineralization in magnetotactic bacteria, focusing on Alphaproteobacteria. To better understand this complex mechanism, we present the four main steps and the main MAPs participating in the process of magnetosome formation.

SUBMITTER: Ben-Shimon S

PROVIDER: S-EPMC8536778 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that form intracellular nanoparticles of magnetite (Fe3O4) or greigite (Fe3S4) in a genetically controlled manner. Magnetite and greigite synthesis requires MTB to transport a large amount of iron from the environment. Most intracellular iron was proposed to be contained within the crystals. However, recent mass spectrometry studies suggest that MTB may contain a large amount of iron that is not precipitated in crystals. Here, we attempted to resolve these discrepancies by performing chemical and magnetic assays to quantify the different iron pools in the magnetite-forming strain Magnetospirillum magneticum AMB-1, as well as in mutant strains showing defects in crystal precipitation, cultivated at various iron concentrations. All results show that magnetite represents at most 30% of the total intracellular iron under our experimental conditions and even less in the mutant strains. We further examined the iron speciation and subcellular localization in AMB-1 using the fluorescent indicator FIP-1, which was designed for the detection of labile Fe(II). Staining with this probe suggests that unmineralized reduced iron is found in the cytoplasm and associated with magnetosomes. Our results demonstrate that, under our experimental conditions, AMB-1 is able to accumulate a large pool of iron distinct from magnetite. Finally, we discuss the biochemical and geochemical implications of these results.IMPORTANCE Magnetotactic bacteria (MTB) produce iron-based intracellular magnetic crystals. They represent a model system for studying iron homeostasis and biomineralization in microorganisms. MTB sequester a large amount of iron in their crystals and have thus been proposed to significantly impact the iron biogeochemical cycle. Several studies proposed that MTB could also accumulate iron in a reservoir distinct from their crystals. Here, we present a chemical and magnetic methodology for quantifying the iron pools in the magnetotactic strain AMB-1. Results showed that most iron is not contained in crystals. We then adapted protocols for the fluorescent Fe(II) detection in bacteria and showed that iron could be detected outside crystals using fluorescence assays. This work suggests a more complex picture for iron homeostasis in MTB than previously thought. Because iron speciation controls its fate in the environment, our results also provide important insights into the geochemical impact of MTB.

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Current view of iron biomineralization in magnetotactic bacteria

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