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Concept: Magnetotactic bacteria

166

The iron oxide mineral magnetite (Fe3O4) is produced by various organisms to exploit magnetic and mechanical properties. Magnetotactic bacteria have become one of the best model organisms for studying magnetite biomineralization, as their genomes are sequenced and tools are available for their genetic manipulation. However, the chemical route by which magnetite is formed intracellularly within the so-called magnetosomes has remained a matter of debate. Here we used X-ray absorption spectroscopy at cryogenic temperatures and transmission electron microscopic imaging techniques to chemically characterize and spatially resolve the mechanism of biomineralization in those microorganisms. We show that magnetite forms through phase transformation from a highly disordered phosphate-rich ferric hydroxide phase, consistent with prokaryotic ferritins, via transient nanometric ferric (oxyhydr)oxide intermediates within the magnetosome organelle. This pathway remarkably resembles recent results on synthetic magnetite formation and bears a high similarity to suggested mineralization mechanisms in higher organisms.

Concepts: DNA, Bacteria, Iron, Organism, Microbiology, Mineral, Magnetite, Magnetotactic bacteria

28

Atomic force microscopy (AFM) was used in concert with transmission electron microscopy (TEM) to image magnetotactic bacteria (Magnetospirillum gryphiswaldense MSR-1 and Magnetospirillum magneticum AMB-1), magnetosomes, and purified Mms6 proteins. Mms6 is a protein that is associated with magnetosomes in M. magneticum AMB-1 and is believed to control the synthesis of magnetite (Fe(3)O(4)) within the magnetosome. We demonstrated how AFM can be used to capture high-resolution images of live bacteria and achieved nanometer resolution when imaging Mms6 protein molecules on magnetite. We used AFM to acquire simultaneous topography and amplitude images of cells that were combined to provide a three-dimensional reconstructed image of M. gryphiswaldense MSR-1. TEM was used in combination with AFM to image M. gryphiswaldense MSR-1 and magnetite-containing magnetosomes that were isolated from the bacteria. AFM provided information, such as size, location and morphology, which was complementary to the TEM images.

Concepts: Protein, Electron, Bacteria, Atom, Transmission electron microscopy, Scanning tunneling microscope, Magnetotaxis, Magnetotactic bacteria

27

Magnetotactic bacteria biosynthesize magnetite nanoparticles of high structural and chemical purity that allow them to orientate in the geomagnetic field. In this work we have followed the process of biomineralization of these magnetite nanoparticles. We have performed a time-resolved study on magnetotactic bacteria Magnetospirillum gryphiswaldense strain MSR-1. From the combination of magnetic and structural studies by means of Fe K-edge X-ray Absorption Near Edge Spectroscopy (XANES) and High-Resolution Transmission Electron Microscopy (HRTEM) we have identified and quantified two phases of Fe (ferrihydrite and magnetite) involved in the biomineralization process, confirming the role of ferrihydrite as the source of Fe ions for magnetite biomineralization in Magnetospirillum gryphiswaldense. We have distinguished two steps in the biomineralization process: the first, in which Fe is accumulated in the form of ferrihydrite, and the second, in which the magnetite is rapidly biomineralized from ferrihydrite. Finally, the XANES analysis suggests that the origin of the ferrihydrite could be at bacterial ferritin cores, characterized by a poorly crystalline structure and high phosphorous content.

Concepts: Electron, Bacteria, Magnetic field, Iron, Magnetism, Magnetite, Magnetotaxis, Magnetotactic bacteria

27

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

Concepts: Experimental design, Bacteria, Statistics, Microbiology, Experiment, Design of experiments, Statistical theory, Magnetotactic bacteria

3

The origin and evolution of magnetoreception, which in diverse prokaryotes and protozoa is known as magnetotaxis and enables these microorganisms to detect Earth’s magnetic field for orientation and navigation, is not well understood in evolutionary biology. The only known prokaryotes capable of sensing the geomagnetic field are magnetotactic bacteria (MTB), motile microorganisms that biomineralize intracellular, membrane-bounded magnetic single-domain crystals of either magnetite (Fe3O4) or greigite (Fe3S4) called magnetosomes. Magnetosomes are responsible for magnetotaxis in MTB. Here we report the first large-scale metagenomic survey of MTB from both northern and southern hemispheres combined with 28 genomes from uncultivated MTB. These genomes expand greatly the coverage of MTB in the Proteobacteria, Nitrospirae, and Omnitrophica phyla, and provide the first genomic evidence of MTB belonging to the Zetaproteobacteria and “Candidatus Lambdaproteobacteria” classes. The gene content and organization of magnetosome gene clusters, which are physically grouped genes that encode proteins for magnetosome biosynthesis and organization, are more conserved within phylogenetically similar groups than between different taxonomic lineages. Moreover, the phylogenies of core magnetosome proteins form monophyletic clades. Together, these results suggest a common ancient origin of iron-based (Fe3O4and Fe3S4) magnetotaxis in the domain Bacteria that underwent lineage-specific evolution, shedding new light on the origin and evolution of biomineralization and magnetotaxis, and expanding significantly the phylogenomic representation of MTB.

Concepts: DNA, Gene, Archaea, Bacteria, Evolution, Organism, Microbiology, Magnetotactic bacteria

2

Magnetotactic bacteria (MTB) play an important role in Earth’s biogeochemical cycles by transporting minerals in aquatic ecosystems, and have shown promise for controlled transport of microscale objects in flow conditions. However, how MTB traverse complex flow environments is not clear. Here, using microfluidics and high-speed imaging, it is revealed that magnetotaxis enables directed motion of Magnetospirillum magneticum over long distances in flow velocities ranging from 2 to 1260 µm s-1 , corresponding to shear rates ranging from 0.2 to 142 s-1 -a range relevant to both aquatic environments and biomedical applications. The ability of MTB to overcome a current is influenced by the flow, the magnetic field, and their relative orientation. MTB can overcome 2.3-fold higher flow velocities when directed to swim perpendicular to the flow as compared to upstream, as the latter orientation induces higher drag. The results indicate a threshold drag of 9.5 pN, corresponding to a flow velocity of 550 µm s-1 , where magnetotaxis enables MTB to overcome counterdirectional flow. These findings bring new insights into the interactions of MTB with complex flow environments relevant to aquatic ecosystems, while suggesting opportunities for in vivo applications of MTB in microbiorobotics and targeted drug delivery.

Concepts: Bacteria, Magnetic field, Magnetism, Special relativity, Systems ecology, Magnetotaxis, Magnetotactic bacteria, Magnetospirillum

2

Magnetotactic bacteria produce chains of membrane-bound organelles that direct the biomineralization of magnetic nanoparticles. These magnetosome compartments are a model for studying the biogenesis and subcellular organization of bacterial organelles. Previous studies have suggested that discrete gene products build and assemble magnetosomes in a stepwise fashion. Here, using an inducible system, we show that the stages of magnetosome formation are highly dynamic and interconnected. During de novo formation, magnetosomes first organize into discontinuous chain fragments that are subsequently connected by the bacterial actin-like protein MamK. We also find that magnetosome membranes are not uniform in size and can grow in a biomineralization-dependent manner. In the absence of biomineralization, magnetosome membranes stall at a diameter of ~50 nm. Those that have initiated biomineralization then expand to significantly larger sizes and accommodate mature magnetic particles. We speculate that such a biomineralization-dependent checkpoint for membrane growth establishes the appropriate conditions within the magnetosome to ensure successful nucleation and growth of magnetic particles.

Concepts: DNA, Bacteria, Microbiology, Cell membrane, Organelle, Initiation, Magnetotaxis, Magnetotactic bacteria

1

The navigation of magnetotactic bacteria relies on specific intracellular organelles, the magnetosomes, which are membrane-enclosed crystals of magnetite aligned into a linear chain. The magnetosome chain acts as a cellular compass, aligning the cells in the geomagnetic field in order to search for suitable environmental conditions in chemically stratified water columns and sediments. During cytokinesis, magnetosome chains have to be properly positioned, cleaved and separated in order to be evenly passed into daughter cells. In Magnetospirillum gryphiswaldense, the assembly of the magnetosome chain is controlled by the actin-like MamK, which polymerizes into cytoskeletal filaments that are connected to magnetosomes through the acidic MamJ protein. MamK filaments were speculated to recruit the magnetosome chain to cellular division sites, thus ensuring equal organelle inheritance. However, the underlying mechanism of magnetic organelle segregation has remained largely unknown.

Concepts: DNA, Protein, Cell nucleus, Cell, Bacteria, Eukaryote, Organelle, Magnetotactic bacteria

1

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 (57)Fe during magnetite biomineralization but not in even Fe isotopes ((54)Fe, (56)Fe, and (58)Fe), 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.

Concepts: Bacteria, Microbiology, Magnetism, Mineral, Geology, Magnetite, Magnetotaxis, Magnetotactic bacteria

1

Magnetotactic bacteria align along the Earth’s magnetic field using an organelle called the magnetosome, a biomineralized magnetite (Fe(ii)Fe(iii)2O4) or greigite (Fe(ii)Fe(iii)2S4) crystal embedded in a lipid vesicle. Although the need for both iron(ii) and iron(iii) is clear, little is known about the biological mechanisms controlling their ratio. Here we present the structure of the magnetosome-associated protein MamP and find that it is built on a unique arrangement of a self-plugged PDZ domain fused to two magnetochrome domains, defining a new class of c-type cytochrome exclusively found in magnetotactic bacteria. Mutational analysis, enzyme kinetics, co-crystallization with iron(ii) and an in vitro MamP-assisted magnetite production assay establish MamP as an iron oxidase that contributes to the formation of iron(iii) ferrihydrite eventually required for magnetite crystal growth in vivo. These results demonstrate the molecular mechanisms of iron management taking place inside the magnetosome and highlight the role of magnetochrome in iron biomineralization.

Concepts: Cell, Archaea, Bacteria, Metabolism, Earth, Magnetism, Magnetite, Magnetotactic bacteria