Primordial magnetotaxis in putative giant paleoproterozoic magnetofossils.

Magnetotactic bacteria produce chains of nanoscopic iron minerals used for navigation, which can be preserved over geological timescales in the form of magnetofossils. Micrometer-sized magnetite crystals with unusual shapes suggesting a biologically controlled mineralization have been found in the geological record and termed giant magnetofossils. The biological origin and function of giant magnetofossils remains unclear, due to the lack of modern analogues to giant magnetofossils. Using distinctive Ptychographic nanotomography data of Precambrian (1.88 Ga) rocks, we recovered the morphology of micrometric cuboid grains of iron oxides embedded in an organic filamentous fossil to construct synthetic magnetosomes. Their morphology is different from that of previously found giant magnetofossils, but their occurrence in filamentous microfossils and micromagnetic simulations support the hypothesis that they could have functioned as a navigation aid, akin to modern magnetosomes.

Large-Scale Cultivation of Magnetotactic Bacteria and the Optimism for Sustainable and Cheap Approaches in Nanotechnology.

Magnetotactic bacteria (MTB), a diverse group of marine and freshwater microorganisms, have attracted the scientific community's attention since their discovery. These bacteria biomineralize ferrimagnetic nanocrystals, the magnetosomes, or biological magnetic nanoparticles (BMNs), in a single or multiple chain(s) within the cell. As a result, cells experience an optimized magnetic dipolar moment responsible for a passive alignment along the lines of the geomagnetic field. Advances in MTB cultivation and BMN isolation have contributed to the expansion of the biotechnological potential of MTB in recent decades. Several studies with mass-cultured MTB expanded the possibilities of using purified nanocrystals and whole cells in nano- and biotechnology. Freshwater MTB were primarily investigated in scaling up processes for the production of BMNs. However, marine MTB have the potential to overcome freshwater species applications due to the putative high efficiency of their BMNs in capturing molecules. Regarding the use of MTB or BMNs in different approaches, the application of BMNs in biomedicine remains the focus of most studies, but their application is not restricted to this field. In recent years, environment monitoring and recovery, engineering applications, wastewater treatment, and industrial processes have benefited from MTB-based biotechnologies. This review explores the advances in MTB large-scale cultivation and the consequent development of innovative tools or processes.

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes.

The most well-recognized magnetoreception behaviour is that of the magnetotactic bacteria (MTB), which synthesize membrane-bounded magnetic nanocrystals called magnetosomes via a biologically controlled process. The magnetic minerals identified in prokaryotic magnetosomes are magnetite (Fe3 O4 ) and greigite (Fe3 S4 ). Magnetosome crystals, regardless of composition, have consistent, species-specific morphologies and single-domain size range. Because of these features, magnetosome magnetite crystals possess specific properties in comparison to abiotic, chemically synthesized magnetite. Despite numerous discoveries regarding MTB phylogeny over the last decades, this diversity is still considered underestimated. Characterization of magnetotactic microorganisms is important as it might provide insights into the origin and establishment of magnetoreception in general, including eukaryotes. Here, we describe the magnetotactic behaviour and characterize the magnetosomes from a flagellated protist using culture-independent methods. Results strongly suggest that, unlike previously described magnetotactic protists, this flagellate is capable of biomineralizing its own anisotropic magnetite magnetosomes, which are aligned in complex aggregations of multiple chains within the cell. This organism has a similar response to magnetic field inversions as MTB. Therefore, this eukaryotic species might represent an early origin of magnetoreception based on magnetite biomineralization. It should add to the definition of parameters and criteria to classify biogenic magnetite in the fossil record.

Uptake and persistence of bacterial magnetite magnetosomes in a mammalian cell line: Implications for medical and biotechnological applications.

Magnetotactic bacteria biomineralize intracellular magnetic nanocrystals surrounded by a lipid bilayer called magnetosomes. Due to their unique characteristics, magnetite magnetosomes are promising tools in Biomedicine. However, the uptake, persistence, and accumulation of magnetosomes within mammalian cells have not been well studied. Here, the endocytic pathway of magnetite magnetosomes and their effects on human cervix epithelial (HeLa) cells were studied by electron microscopy and high spatial resolution nano-analysis techniques. Transmission electron microscopy of HeLa cells after incubation with purified magnetosomes showed the presence of magnetic nanoparticles inside or outside endosomes within the cell, which suggests different modes of internalization, and that these structures persisted beyond 120 h after internalization. High-resolution transmission electron microscopy and electron energy loss spectra of internalized magnetosome crystals showed no structural or chemical changes in these structures. Although crystal morphology was preserved, iron oxide crystalline particles of approximately 5 nm near internalized magnetosomes suggests that minor degradation of the original mineral structures might occur. Cytotoxicity and microscopy analysis showed that magnetosomes did not result in any apparent effect on HeLa cells viability or morphology. Based on our results, magnetosomes have significant biocompatibility with mammalian cells and thus have great potential in medical, biotechnological applications.

Applications of Magnetotactic Bacteria, Magnetosomes and Magnetosome Crystals in Biotechnology and Nanotechnology: Mini-Review.

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.

Fingerprints of partial oxidation of biogenic magnetite from cultivated and natural marine magnetotactic bacteria using synchrotron radiation.

Magnetotactic bacteria are a multi-phyletic group of bacteria that synthesize membrane-bound magnetic minerals. Understanding the preservation of these minerals in various environments (e.g., with varying oxygen concentrations and iron supply) is important for understanding their role as carriers of primary magnetizations in sediments and sedimentary rocks. Here we present X-ray near edge structure (XANES) spectra for Fe in magnetotactic bacteria samples from recent sediments to assess surface oxidation and crystal structure changes in bacterial magnetite during early burial. Our results are compared with a XANES spectrum of cultivated Magnetofaba australis samples, and with magnetic properties, and indicate that oxidation of magnetite to maghemite increases with depth in the sediment due to longer exposure to molecular oxygen. These results are relevant to understanding magnetic signatures carried by magnetofossils in oxic sediments and sedimentary rocks of different ages.

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

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.

Ultrastructure of ellipsoidal magnetotactic multicellular prokaryotes depicts their complex assemblage and cellular polarity in the context of magnetotaxis.

Magnetotactic multicellular prokaryotes (MMPs) consist of unique microorganisms formed by genetically identical Gram-negative bacterial that live as a single individual capable of producing magnetic nano-particles called magnetosomes. Two distinct morphotypes of MMPs are known: spherical MMPs (sMMPs) and ellipsoidal MMPs (eMMPs). sMMPs have been extensively characterized, but less information exists for eMMPs. Here, we report the ultrastructure and organization as well as gene clusters responsible for magnetosome and flagella biosynthesis in the magnetite magnetosome producer eMMP Candidatus Magnetananas rongchenensis. Transmission electron microscopy and focused ion beam scanning electron microscopy (FIB-SEM) 3D reconstruction reveal that cells with a conspicuous core-periphery polarity were organized around a central space. Magnetosomes were organized in multiple chains aligned along the periphery of each cell. In the partially sequenced genome, magnetite-related mamAB gene and mad gene clusters were identified. Two cell morphologies were detected: irregular elliptical conical 'frustum-like' (IECF) cells and H-shaped cells. IECF cells merge to form H-shaped cells indicating a more complex structure and possibly a distinct evolutionary position of eMMPs when compared with sMMPs considering multicellularity.

Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment.

BACKGROUND: Magnetotactic bacteria (MTB) are a unique group of prokaryotes that have a potentially high impact on global geochemical cycling of significant primary elements because of their metabolic plasticity and the ability to biomineralize iron-rich magnetic particles called magnetosomes. Understanding the genetic composition of the few cultivated MTB along with the unique morphological features of this group of bacteria may provide an important framework for discerning their potential biogeochemical roles in natural environments. RESULTS: Genomic and ultrastructural analyses were combined to characterize the cultivated magnetotactic coccus Magnetofaba australis strain IT-1. Cells of this species synthesize a single chain of elongated, cuboctahedral magnetite (Fe3O4) magnetosomes that cause them to align along magnetic field lines while they swim being propelled by two bundles of flagella at velocities up to 300 µm s-1. High-speed microscopy imaging showed the cells move in a straight line rather than in the helical trajectory described for other magnetotactic cocci. Specific genes within the genome of Mf. australis strain IT-1 suggest the strain is capable of nitrogen fixation, sulfur reduction and oxidation, synthesis of intracellular polyphosphate granules and transporting iron with low and high affinity. Mf. australis strain IT-1 and Magnetococcus marinus strain MC-1 are closely related phylogenetically although similarity values between their homologous proteins are not very high. CONCLUSION: Mf. australis strain IT-1 inhabits a constantly changing environment and its complete genome sequence reveals a great metabolic plasticity to deal with these changes. Aside from its chemoautotrophic and chemoheterotrophic metabolism, genomic data indicate the cells are capable of nitrogen fixation, possess high and low affinity iron transporters, and might be capable of reducing and oxidizing a number of sulfur compounds. The relatively large number of genes encoding transporters as well as chemotaxis receptors in the genome of Mf. australis strain IT-1 combined with its rapid swimming velocities, indicate that cells respond rapidly to environmental changes.

Cell adhesion, multicellular morphology, and magnetosome distribution in the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis.

Candidatus Magnetoglobus multicellularis is an uncultured magnetotactic multicellular prokaryote composed of 17-40 Gram-negative cells that are capable of synthesizing organelles known as magnetosomes. The magnetosomes of Ca. M. multicellularis are composed of greigite and are organized in chains that are responsible for the microorganism's orientation along magnetic field lines. The characteristics of the microorganism, including its multicellular life cycle, magnetic field orientation, and swimming behavior, and the lack of viability of individual cells detached from the whole assembly, are considered strong evidence for the existence of a unique multicellular life cycle among prokaryotes. It has been proposed that the position of each cell within the aggregate is fundamental for the maintenance of its distinctive morphology and magnetic field orientation. However, the cellular organization of the whole organism has never been studied in detail. Here, we investigated the magnetosome organization within a cell, its distribution within the microorganism, and the intercellular relationships that might be responsible for maintaining the cells in the proper position within the microorganism, which is essential for determining the magnetic properties of Ca. M. multicellularis during its life cycle. The results indicate that cellular interactions are essential for the determination of individual cell shape and the magnetic properties of the organism and are likely directly associated with the morphological changes that occur during the multicellular life cycle of this species.

Optimization of magnetosome production and growth by the magnetotactic vibrio Magnetovibrio blakemorei strain MV-1 through a statistics-based experimental design.

The growth and magnetosome production of the marine magnetotactic vibrio Magnetovibrio blakemorei strain MV-1 were optimized through a statistics-based experimental factorial design. In the optimized growth medium, maximum magnetite yields of 64.3 mg/liter in batch cultures and 26 mg/liter in a bioreactor were obtained.