Magnetotactic bacteria accumulate a large pool of iron distinct from their magnetite crystals

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 which is subsequently concentrated in organelles called magnetosomes for crystal precipitation and maturation. X-ray absorption analysis of MTB suggests that the intracellular iron is mainly contained within the crystals, thus preventing potential toxic effects of free iron. In contrast, recent mass spectrometry studies suggest that MTB may contain a large amount of iron that is not precipitated in crystals. Here, we attempt to resolve these descrepancies by performing chemical and magnetic assays to quantify the different iron pools in the magnetite-forming strain Magnetospirillum magneticum AMB-1 cultivated at varying iron concentrations. AMB-1 mutants showing defects in crystal precipitation were also characterized following the same approach. All results show that magnetite represents at most 30 % of the total intracellular iron under our experimental conditions. We further examined the iron speciation and subcellular localization in AMB-1 using the fluorescent indicator FIP-1 that is designed for 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.