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Cellular iron homeostasis is vital and maintained through tight regulation of iron import, efflux, storage and detoxification 1 – 3 . The most common modes of iron storage use proteinaceous compartments, such as ferritins and related proteins 4 , 5 . Although lipid-bounded iron compartments have also been described, the basis for their formation and function remains unknown 6 , 7 . Here we focus on one such compartment, herein named the ‘ferrosome’, that was previously observed in the anaerobic bacterium Desulfovibrio magneticus 6 . Using a proteomic approach, we identify three ferrosome-associated (Fez) proteins that are responsible for forming ferrosomes in D .  magneticus . Fez proteins are encoded in a putative operon and include FezB, a P 1B-6 -ATPase found in phylogenetically and metabolically diverse species of bacteria and archaea. We show that two other bacterial species, Rhodopseudomonas palustris and Shewanella putrefaciens , make ferrosomes through the action of their six-gene fez operon. Additionally, we find that fez operons are sufficient for ferrosome formation in foreign hosts. Using S .  putrefaciens as a model, we show that ferrosomes probably have a role in the anaerobic adaptation to iron starvation. Overall, this work establishes ferrosomes as a new class of iron storage organelles and sets the stage for studying their formation and structure in diverse microorganisms. A fez gene cluster drives formation of ferrosomes, a distinct lipid-bounded organelle for iron storage, in diverse bacterial species.

Magnetotactic bacteria perform biomineralization of intracellular magnetite (Fe₃O₄) nanoparticles. Although they may be among the earliest microorganisms capable of biomineralization on Earth, identifying their activity in ancient sedimentary rocks remains challenging because of the lack of a reliable biosignature. We determined Fe isotope fractionations by the magnetotactic bacterium Magnetospirillum magneticum AMB-1. The AMB-1 strain produced magnetite strongly depleted in heavy Fe isotopes, by 1.5 to 2.5 per mil relative to the initial growth medium. Moreover, we observed mass-independent isotope fractionations in ⁵⁷Fe during magnetite biomineralization but not in even Fe isotopes (⁵⁴Fe, ⁵⁶Fe, and ⁵⁸Fe), highlighting a magnetic isotope effect. This Fe isotope anomaly provides a potential biosignature for the identification of magnetite produced by magnetotactic bacteria in the geological record.

Magnetotactic bacteria are a diverse group of microorganisms that use intracellular chains of ferrimagnetic nanocrystals, produced within magnetosome organelles, to align and navigate along the geomagnetic field. Several conserved genes for magnetosome formation have been described, but the mechanisms leading to distinct species-specific magnetosome chain configurations remain unclear. Here, we show that the fragmented nature of magnetosome chains in Magnetospirillum magneticum AMB-1 is controlled by genes mcaA and mcaB . McaA recognizes the positive curvature of the inner cell membrane, while McaB localizes to magnetosomes. Along with the MamK actin-like cytoskeleton, McaA and McaB create space for addition of new magnetosomes in between pre-existing magnetosomes. Phylogenetic analyses suggest that McaA and McaB homologs are widespread among magnetotactic bacteria and may represent an ancient strategy for magnetosome positioning. Magnetotactic bacteria use intracellular chains of ferrimagnetic nanocrystals, produced within magnetosome organelles, to align and navigate along the geomagnetic field. Here, Wan et al. identify two proteins involved in magnetosome positioning in Magnetospirillum magneticum , homologs of which are widespread among magnetotactic bacteria.

The demand for characterisation of beam-sensitive samples at the nanoscale in environmental conditions is increasing for applications in materials science and biology. Here we communicate a protocol with custom software, enabling precise control over the electron microscope, and a custom sample holder, facilitating automated acquisition of fast 3D data from a single object under environmental conditions. This method enables imaging with a controlled electron dose and multi-modal electron signals. The method can be used in environmental scanning or transmission electron microscopes for easy sample preparation and to benefit from high spatial resolution, respectively. To demonstrate its effectiveness, we investigate the porosity of Al(OH) 3 hydrogels, and the penetration ability and distribution of gold nanoparticles. Unfixed, hydrated magnetotactic bacteria producing intracellular iron oxide nanoparticles were also characterized in 3D in their native state. This methodological and technical development serves as a milestone in the study of various samples at any humidity level, offering easier sample preparation compared to cryo-TEM techniques, while maintaining a similar or even lower dose level. Louis-Marie Lebas and colleagues present a method for fast 3D electron microscopy of sensitive samples in environmental conditions using custom software and hardware. It enables automated, low-dose imaging with high resolution and simple preparation.

The introduction of various iron-chelating agents to the Magnetospirillum magneticum strain AMB-1 bacterial growth medium stimulated the growth of M. magneticum strain AMB-1 magnetotactic bacteria and enhanced the production of magnetosomes. After 7 days of growth, the number of bacteria and the production of magnetosomes were increased in the presence of iron-chelating agents by factors of up to 2 and 6, respectively. The presence of iron-chelating agents also produced an increase in magnetosome size and chain length and yielded improved magnetosome heating properties. The specific absorption rate of suspensions of magnetosome chains isolated from M. magneticum strain AMB-1 magnetotactic bacteria, measured under the application of an alternating magnetic field of average field strength 20 mT and frequency 198 kHz, increased from 222 W/g^sub Fe^ in the absence of iron-chelating agent up to 444 W/g^sub Fe^ in the presence of 4 μM rhodamine B and to 723 W/g^sub Fe^ in the presence of 4 μM EDTA. These observations were made at an iron concentration of 20 μM and iron-chelating agent concentrations below 40 μM.[PUBLICATION ABSTRACT]

Significance Magnetite precipitates through either abiotic or biotic processes. Magnetotactic bacteria synthesize nanosized magnetite intracellularly and may represent one of the most ancient biomineralizing organisms. Thus, identifying bacterial magnetofossils in ancient sediments remains a key point to constrain life evolution over geological times. Although electron microscopy and magnetic characterizations allow identification of recent bacterial magnetofossils, sediment aging leads to variable dissolution or alteration of magnetite, potentially yielding crystals that barely preserve their structural integrity. Thus, reliable biosignatures surviving such modifications are still needed for distinguishing biogenic from abiotic magnetite. Here, we performed magnetotactic bacteria cultures and laboratory syntheses of abiotic magnetites. We quantified trace element incorporation into both types of magnetite, which allowed us to establish criteria for biomagnetite identification. There are longstanding and ongoing controversies about the abiotic or biological origin of nanocrystals of magnetite. On Earth, magnetotactic bacteria perform biomineralization of intracellular magnetite nanoparticles under a controlled pathway. These bacteria are ubiquitous in modern natural environments. However, their identification in ancient geological material remains challenging. Together with physical and mineralogical properties, the chemical composition of magnetite was proposed as a promising tracer for bacterial magnetofossil identification, but this had never been explored quantitatively and systematically for many trace elements. Here, we determine the incorporation of 34 trace elements in magnetite in both cases of abiotic aqueous precipitation and of production by the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1. We show that, in biomagnetite, most elements are at least 100 times less concentrated than in abiotic magnetite and we provide a quantitative pattern of this depletion. Furthermore, we propose a previously unidentified method based on strontium and calcium incorporation to identify magnetite produced by magnetotactic bacteria in the geological record.

Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that biomineralize dissolved iron from the environment into intracellular nanoparticles of magnetite [Fe(II)Fe(III)2O4] or greigite [Fe(II)Fe(III)2S4] in a genetically controlled manner. After cell death, these magnetite and greigite crystals are trapped into sediments which effectively removes iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits nitrogen fixation and primary productivity. Although MTB are ubiquitous in the environment, their impact on the biogeochemical cycling of metallic elements is still poorly constrained. A thorough assessment of the mass of iron incorporated by MTB has been hampered by a lack of methodology to accurately measure the amount of, and variability in, their intracellular iron content. Here, we quantify the mass of iron contained in single MTB cells of the model organism, Magnetospirillum magneticum sp. AMB-1, using a time-resolved mass spectrometry methodology. Bacterial iron content depends on the external iron concentration, and reaches a maximum value of 10-6 ng of iron per cell when bacteria are cultivated with initial iron concentrations of 100 μM or higher. From our experimental results, we calculated the flux of dissolved iron incorporation into natural MTB populations and conclude that MTB may mineralize a significant fraction of environmental dissolved iron into crystals.

Magnetotactic bacteria (MTB) are a diverse group of microorganisms that use intracellular chains of ferrimagnetic nanocrystals, produced within their magnetosome organelles, to align and navigate along the geomagnetic field. The cell biological and biochemical properties of magnetosomes make them a powerful model for studying the molecular mechanisms of biomineralization and compartmentalization in bacteria. While several conserved magnetosome formation genes have been described, the evolutionary strategies for their species-specific diversification remain unknown. Here, we demonstrate that the fragmented nature of magnetosome chains in Magnetospirillum magneticum AMB-1 is controlled by two genes named mcaA and mcaB. McaA recognizes the positive curvature of the inner cell membrane while McaB localises to magnetosomes. Along with the MamK actin-like cytoskeleton, they create space for addition of new magnetosomes in between pre-existing magnetosomes. Phylogenetic analyses suggest that McaAB homologs are widespread and may represent an ancient strategy for organelle positioning in MTB.