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Biomineralization is an elaborate process that controls the deposition of inorganic materials in living organisms with the aid of associated proteins. Magnetotactic bacteria mineralize magnetite (Fe3O4) nanoparticles with finely tuned morphologies in their cells. Mms6, a magnetosome membrane specific (Mms) protein isolated from the surfaces of bacterial magnetite nanoparticles, plays an important role in regulating the magnetite crystal morphology. Although the binding ability of Mms6 to magnetite nanoparticles has been speculated, the interactions between Mms6 and magnetite crystals have not been elucidated thus far. Here, we show a direct adsorption ability of Mms6 on magnetite nanoparticles in vitro. An adsorption isotherm indicates that Mms6 has a high adsorption affinity (Kd = 9.52 µM) to magnetite nanoparticles. In addition, Mms6 also demonstrated adsorption on other inorganic nanoparticles such as titanium oxide, zinc oxide, and hydroxyapatite. Therefore, Mms6 can potentially be utilized for the bioconjugation of functional proteins to inorganic material surfaces to modulate inorganic nanoparticles for biomedical and medicinal applications.

The ability to sense Earth’s magnetic field has evolved in various taxa. However, despite great efforts to find the ‘ magnetic-sensor ’ in vertebrates, the results of these scientific efforts remain inconclusive. A few decades ago, it was found that bacteria, known as magnetotactic bacteria (MTB), can move along a magnetic field using nanometric chain-like structures. Still, it is not fully clear why these bacteria evolved to have this capacity. Thus, while for MTB the ‘ magnetic-sensor ’ is known but the adaptive value is still under debate, for metazoa it is the other way around. In the absence of convincing evidence for any ‘ magnetic-sensor ’ in metazoan species sensitive to Earth’s magnetic field, we hypothesize that a mutualism between these species and MTB provides one. In this relationship the host benefits from a magnetotactic capacity, while the bacteria benefit a hosting environment and dispersal. We provide support for this hypothesis using existing literature, demonstrating that by placing the MTB as the ‘ magnetic-sensor ’, previously contradictory results are now in agreement. We also propose plausible mechanisms and ways to test the hypothesis. If proven correct, this hypothesis would shed light on the forces driving both animal and bacteria magnetotactic abilities.

Magnetotactic bacteria (MTB) biomineralize magnetosomes, which are defined as intracellular nanocrystals of the magnetic minerals magnetite (Fe3O4) or greigite (Fe3S4) enveloped by a phospholipid bilayer membrane. The synthesis of magnetosomes is controlled by a specific set of genes that encode proteins, some of which are exclusively found in the magnetosome membrane in the cell. Over the past several decades, interest in nanoscale technology (nanotechnology) and biotechnology has increased significantly due to the development and establishment of new commercial, medical and scientific processes and applications that utilize nanomaterials, some of which are biologically derived. One excellent example of a biological nanomaterial that is showing great promise for use in a large number of commercial and medical applications are bacterial magnetite magnetosomes. Unlike chemically-synthesized magnetite nanoparticles, magnetosome magnetite crystals are stable single-magnetic domains and are thus permanently magnetic at ambient temperature, are of high chemical purity, and display a narrow size range and consistent crystal morphology. These physical/chemical features are important in their use in biotechnological and other applications. Applications utilizing magnetite-producing MTB, magnetite magnetosomes and/or magnetosome magnetite crystals include and/or involve bioremediation, cell separation, DNA/antigen recovery or detection, drug delivery, enzyme immobilization, magnetic hyperthermia and contrast enhancement of magnetic resonance imaging. Metric analysis using Scopus and Web of Science databases from 2003 to 2018 showed that applied research involving magnetite from MTB in some form has been focused mainly in biomedical applications, particularly in magnetic hyperthermia and drug delivery.

Magnetotactic bacteria are a group of Gram-negative bacteria that synthesize magnetic crystals, enabling them to navigate in relation to magnetic field lines. Morphologies of magnetotactic bacteria include spirillum, coccoid, rod, vibrio, and multicellular morphotypes. The coccid shape is generally the most abundant morphotype among magnetotactic bacteria. Here we describe a species of giant rod-shaped magnetotactic bacteria (designated QR-1) collected from sediment in the low tide zone of Huiquan Bay (Yellow Sea, China). This morphotype accounted for 90% of the magnetotactic bacteria collected, and the only taxonomic group which was detected in the sampling site. Microscopy analysis revealed that QR-1 cells averaged (6.71±1.03)×(1.54±0.20) μm in size, and contained in each cell 42–146 magnetosomes that are arranged in a bundle formed one to four chains along the long axis of the cell. The QR-1 cells displayed axial magnetotaxis with an average velocity of 70±28 μm/s. Transmission electron microscopy based analysis showed that QR-1 cells had two tufts of flagella at each end. Phylogenetic analysis of the 16S rRNA genes revealed that QR-1 together with three other rod-shaped uncultivated magnetotactic bacteria are clustered into a deep branch of Alphaproteobacteria .

Magnetic targeting is one of the most promising approaches for improving the targeting efficiency by which magnetic drug carriers are directed using external magnetic fields to reach their targets. As a natural magnetic nanoparticle (MNP) of biological origin, the magnetosome is a special “organelle” formed by biomineralization in magnetotactic bacteria (MTB) and is essential for MTB magnetic navigation to respond to geomagnetic fields. The magnetic targeting of magnetosomes, however, can be hindered by the aggregation and precipitation of magnetosomes in water and biological fluid environments due to the strong magnetic attraction between particles. In this study, we constructed a magnetosome-like nanoreactor by introducing MTB Mms6 protein into a reverse micelle system. MNPs synthesized by thermal decomposition exhibit the same crystal morphology and magnetism (high saturation magnetization and low coercivity) as natural magnetosomes but have a smaller particle size. The DSPE-mPEG–coated magnetosome-like MNPs exhibit good monodispersion, penetrating the lesion area of a tumor mouse model to achieve magnetic enrichment by an order of magnitude more than in the control groups, demonstrating great prospects for biomedical magnetic targeting applications.

Magnetosomes are lipid-bound organelles that direct the biomineralization of magnetic nanoparticles in magnetotactic bacteria. Magnetosome membranes are not uniform in size and can grow in a biomineralization-dependent manner. However, the underlying mechanisms of magnetosome membrane growth regulation remain unclear. Using cryoelectron tomography, we systematically examined mutants with defects at various stages of magnetosome formation to identify factors involved in controlling membrane growth. We found that a conserved serine protease, MamE, plays a key role in magnetosome membrane growth regulation. When the protease activity of MamE is disrupted, magnetosome membrane growth is restricted, which, in turn, limits the size of the magnetite particles. Consistent with this finding, the upstream regulators of MamE protease activity, MamO and MamM, are also required for magnetosome membrane growth. We then used a combination of candidate and comparative proteomics approaches to identify Mms6 and MamD as two MamE substrates. Mms6 does not appear to participate in magnetosome membrane growth. However, in the absence of MamD, magnetosome membranes grow to a larger size than the wild type. Furthermore, when the cleavage of MamD by MamE protease is blocked, magnetosome membrane growth and biomineralization are severely inhibited, phenocopying the MamE protease-inactive mutant. We therefore propose that the growth of magnetosome membranes is controlled by a protease-mediated switch through processing of MamD. Overall, our work shows that, like many eukaryotic systems, bacteria control the growth and size of biominerals by manipulating the physical properties of intracellular organelles.

Low‐temperature hydrothermal fluids in crustal rocks of the Clarion‐Clipperton‐Zone (East Pacific) supply dissolved oxygen into the sediment from below. Diffusive upward transport led to formation of an inverse oxygen gradient zone in the overlying sediments. The resultant oxic/suboxic transition zone could provide suitable conditions for a deep, mirrored habitat for microaerophilic magnetotactic bacteria that were so far only found in the shallow oxygen gradient zone beneath the sediment‐water interface. Previously, the presence of such deep‐living MTB was only inferred from paleo‐ and rock‐magnetic proxies, but here it is evidenced by electron microscopy showing intact multi‐stranded, large (>120 nm diameter) magnetofossil chains from the deep past oxic/suboxic transition zone. Sediment magnetic parameters indicate localized zones of biogenic magnetite accumulation affirming the existence of living MTB at around 8 m sediment depth. This finding is the first evidence for MTB in bottom‐up oxygenated sediments near the sediment/crust interface. Plain Language Summary Biogeochemical processes in sediments at the ocean floor consume oxygen dissolved in pore waters, resulting in anoxic conditions in deeper sediment layers. However, in young, tectonically active parts as in the eastern Pacific oceanic crust, seawater can enter and flow through the permeable rocks that form the crystalline base of the seafloor and thereby supply oxygen into the overlying sediment column from below. This process was shown to create an oxic zone within deep sediments that may be populated by so‐called “magnetotactic” bacteria, which require small amounts of oxygen and therefore usually live just beneath the sediment surface. It was not thought possible so far that such mobile bacteria could also live in deeper subsurface sediments. These bacteria produce magnetic particles, which they use as a compass. Known as “magnetofossils,” these tiny particles can be preserved in marine sediments for millions of years. We could detect fresh “magnetofossils” in very old deep sediments with specialized microscopes and magnetic measurements. These deep‐living bacteria thus inhabit a “mirror‐world,” where their necessary oxygen supply comes from below, not from above. Their compass should therefore be oriented in the opposite vertical direction to their shallow‐living analogs. Key Points Fresh magnetosome chains of magnetotactic bacteria were detected in deep oxygen‐gradient zone near (<15 m) the sediment/crust interface Selective magnetic parameters reveal microbial activity in past oxic/suboxic transition zones of bottom‐up oxygenated sediments Oxygen‐rich low‐temperature hydrothermal fluids in young oceanic crust can support microaerophilic life in the overlying bottom sediment

The scientific community’s interest in magnetotactic bacteria has increased substantially in recent decades. These prokaryotes have the particularity of synthesizing nanomagnets, called magnetosomes. The majority of research is based on several scientific questions. Where do magnetotactic bacteria live, what are their characteristics, and why are they magnetic? What are the molecular phenomena of magnetosome biomineralization and what are the physical characteristics of magnetosomes? In addition to scientific curiosity to better understand these stunning organisms, there are biotechnological opportunities to consider. Magnetotactic bacteria, as well as magnetosomes, are used in medical applications, for example cancer treatment, or in environmental ones, for example bioremediation. In this mini-review, we investigated all the aspects mentioned above and summarized the currently available knowledge.

Characterizing the chemistry and magnetism of magnetotactic bacteria (MTB) is an important aspect of understanding the biomineralization mechanism and function of the chains of magnetosomes (Fe₃O₄ nanoparticles) found in such species. Images and X-ray absorption spectra (XAS) of magnetosomes extracted from, and magnetosomes in, whole Magnetovibrio blakemorei strain MV-1 cells have been recorded using soft X-ray ptychography at the Fe 2p edge. A spatial resolution of 7 nm is demonstrated. Precursor-like and immature magnetosome phases in a whole MV-1 cell were visualized, and their Fe 2p spectra were measured. Based on these results, a model for the pathway of magnetosome biomineralization for MV-1 is proposed. Fe 2p X-ray magnetic circular dichroism (XMCD) spectra have been derived from ptychography image sequences recorded using left and right circular polarization. The shape of the XAS and XMCD signals in the ptychographic absorption spectra of both sample types is identical to the shape and signals measured with conventional bright-field scanning transmission X-ray microscope. A weaker and inverted XMCD signal was observed in the ptychographic phase spectra of the extracted magnetosomes. The XMCD ptychographic phase spectrum of the intracellular magnetosomes differed from the ptychographic phase spectrum of the extracted magnetosomes. These results demonstrate that spectro-ptychography offers a superior means of characterizing the chemical and magnetic properties of MTB at the individual magnetosome level.

Near-shore marine sediments deposited during the Paleocene–Eocene Thermal Maximum at Wilson Lake, NJ, contain abundant conventional and giant magnetofossils. We find that giant, needle-shaped magnetofossils from Wilson Lake produce distinct magnetic signatures in low-noise, high-resolution first-order reversal curve (FORC) measurements. These magnetic measurements on bulk sediment samples identify the presence of giant, needle-shaped magnetofossils. Our results are supported by micromagnetic simulations of giant needle morphologies measured from transmission electron micrographs of magnetic extracts from Wilson Lake sediments. These simulations underscore the single-domain characteristics and the large magnetic coercivity associated with the extreme crystal elongation of giant needles. Giant magnetofossils have so far only been identified in sediments deposited during global hyperthermal events and therefore may serve as magnetic biomarkers of environmental disturbances. Our results show that FORC measurements are a nondestructive method for identifying giant magnetofossil assemblages in bulk sediments, which will help test their ecology and significance with respect to environmental change.