Richard B. Frankel

Magnetosome formation in prokaryotes

Magnetotactic bacteria were discovered almost 30 years ago, and for many years and many different reasons, the number of researchers working in this field was few and progress was slow. Recently, however, thanks to the isolation of new strains and the development of new techniques for manipulating these strains, researchers from several laboratories have made significant progress in elucidating the molecular, biochemical, chemical and genetic bases of magnetosome formation and understanding how these unique intracellular organelles function. We focus here on this progress.

Magnetite in Freshwater Magnetotactic Bacteria

A previously undescribed magnetotactic spirillum isolated from a freshwater swamp was mass cultured in the magnetic as well as the nonmagnetic state in chemically defined culture media. Results of Mossbauer spectroscopic analysis applied to whole cells identifies magnetite as a constituent of these magnetic bacteria.

Rock magnetic criteria for the detection of biogenic magnetite

Abstract We report results on the magnetic properties of magnetites produced by magnetotactic and dissimilatory iron-reducing bacteria. Magnetotactic bacterial (MTB) strains MS1, MV1 and MV2 and dissimilatory iron-reducing bacterium strain GS-15, grown in pure cultures, were used in this study. Our results suggest that a combination of room temperature coercivity analysis and low temperature remanence measurements provides a characteristic magnetic signature for intact chains of single domain (SD) particles of magnetite from MTBs. The most useful magnetic property measurements include: (1) acquisition and demagnetization of isothermal remanent magnetization (IRM) using static, pulse and alternating fields; (2) acquisition of anhysteretic remanent magnetization (ARM); and (3) thermal dependence of low temperature (20 K) saturation IRM after cooling in zero field (ZFC) or in a 2.5 T field (FC) from 300 K. However, potentially the most diagnostic magnetic parameter for magnetosome chain identification in bulk sediment samples is related to the difference between low temperature zero-field and field cooled SIRMs on warming through the Verwey transition (T ≈ 100 K). Intact chains of unoxidized magnetite magnetosomes have ratios of δFC/δZFC greater than 2, where the parameter δ is a measure of the amount of remanence lost by warming through the Verwey transition. Disruption of the chain structure or conversion of the magnetosomes to maghemite reduces the δFC/δZFC ratio to around 1, similar to values observed for some inorganic magnetite, maghemite, greigite and GS-15 particles. Numerical simulations of δFC/δZFC ratios for simple binary mixtures of magnetosome chains and inorganic magnetic fractions suggest that the δFC/δZFC parameter can be a sensitive indicator of biogenic magnetite in the form of intact chains of magnetite magnetosomes and can be a useful magnetic technique for identifying them in whole-sediment samples. The strength of our approach lies in the comparative ease and rapidity with which magnetic measurements can be made, compared to techniques such as electron microscopy.

Magneto-Aerotaxis in Marine Coccoid Bacteria

Magnetotactic cocci swim persistently along local magnetic field lines in a preferred direction that corresponds to downward migration along geomagnetic field lines. Recently, high cell concentrations of magnetotactic cocci have been found in the water columns of chemically stratified, marine and brackish habitats, and not always in the sediments, as would be expected for persistent, downward-migrating bacteria. Here we report that cells of a pure culture of a marine magnetotactic coccus, designated strain MC-1, formed microaerophilic bands in capillary tubes and used aerotaxis to migrate to a preferred oxygen concentration in an oxygen gradient. Cells were able to swim in either direction along the local magnetic field and used magnetotaxis in conjunction with aerotaxis, i.e., magnetically assisted aerotaxis, or magneto-aerotaxis, to more efficiently migrate to and maintain position at their preferred oxygen concentration. Cells of strain MC-1 had a novel, aerotactic sensory mechanism that appeared to function as a two-way switch, rather than the temporal sensory mechanism used by other bacteria, including Magnetospirillum megnetotacticum, in aerotaxis. The cells also exhibited a response to short-wavelength light (< or = 500 nm), which caused them to swim persistently parallel to the magnetic field during illumination.

Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications.

Abstract Magnetotactic bacteria orient and migrate along geomagnetic field lines. This ability is based on intracellular magnetic structures, the magnetosomes, which comprise nanometer-sized, membrane-bound crystals of the magnetic iron minerals magnetite (Fe3O4) or greigite (Fe3S4). Magnetosome formation is achieved by a mineralization process with biological control over the accumulation of iron and the deposition of the mineral particle with specific size and orientation within a membrane vesicle at specific locations in the cell. This review focuses on the current knowledge about magnetotactic bacteria and will outline aspects of the physiology and molecular biology of the biomineralization process. Potential biotechnological applications of magnetotactic bacteria and their magnetosomes as well as perspectives for further research are discussed.

Anaerobic Magnetite Production by a Marine, Magnetotactic Bacterium

Bacterial production of magnetite represents a significant contribution to the natural remanent magnetism of deep-sea and other sediments1–5. Because cells of the freshwater magnetotactic bacterium Aquaspirillum magnetotacticum require molecular oxygen for growth and magnetite synthesis6, production of magnetite by magnetotactic bacteria has been considered to occur only in surficial aerobic sediments7. Moreover, it has been suggested that deposits of single-domain magnetite crystals are palaeooxygen indicators presumably having been formed under predominantly microaerobic conditions5–8. In contrast, some nonmagnetotactic, dissimilatory iron-reducing bacteria, such as the recently described strain GS-15 by Lovley et al.7, synthesize extracellular magnetite from hydrous ferric oxide under anaerobic conditions. We now report the first isolation and axenic culture of a marine, magnetotactic bacterium, designated MV-1, that can synthesize intracellular, single-domain magnetite crystals under strictly anaerobic conditions. We conclude that magnetotactic bacteria do not necessarily require molecular oxygen for magnetite synthesis and suggest that they, as well as dissimilatory iron-reducing bacteria, can contribute to the natural remanent magnetism of even long-term anaerobic sediments.

Biologically Induced Mineralization by Bacteria

Bacteria are small, prokaryotic, microorganisms that are ubiquitous in surface and subsurface terrestrial and aquatic habitats. Prokaryotes comprise two Domains (Superkingdoms) in the biological taxonomic hierarchy, the Bacteria and the Archaea. They exhibit remarkable diversity both genetically and metabolically even within the same microenvironment and they are thought to play a major role in the deposition and weathering of minerals in the earth’s crust. The synthesis of minerals by prokaryotes can be grouped into two canonical modes: 1) biologically induced mineralization (BIM) and 2) biologically controlled mineralization (BCM) (Lowenstam 1981; Lowenstam and Weiner 1989). In this chapter, we focus on biologically induced mineralization. Minerals that form by biologically induced mineralization processes generally nucleate and grow extracellularly as a result of metabolic activity of the organism and subsequent chemical reactions involving metabolic byproducts. In many cases , the organisms secrete one or more metabolic products that react with ions or compounds in the environment resulting in the subsequent deposition of mineral particles. Thus, BIM is a presumably unintended and uncontrolled consequence of metabolic activities. The minerals that form are often characterized by poor crystallinity , broad particle-size distributions, and lack of specific crystal morphologies. In addition , the lack of control over mineral formation often results in poor mineral specificity and/or the inclusion of impurities in the mineral lattice. BIM is, in essence, equivalent to inorganic mineralization under the same environmental conditions and the minerals are therefore likely to have crystallochemical features that are generally indistinguishable from minerals produced by inorganic chemical reactions. In some cases, the metabolic products diffuse away and minerals form from solution. However , bacterial surfaces such as cell walls or polymeric materials (exopolymers) exuded by bacteria, including slimes, sheaths, or biofilms, and even dormant spores, can act as important sites for the adsorption of ions …

Multiple Evolutionary Origins of Magnetotaxis in Bacteria

Magnetosomes are intracellular, iron-rich, membrane-enclosed magnetic particles that allow magnetotactic bacteria to orient in the earths geomagnetic field as they swim. The magnetosomes of most magnetotactic bacteria contain iron oxide particles, but some magnetotactic species contain iron sulfide particles instead. Phylogenetic analyses of small subunit ribosomal RNA sequences showed that all known magnetotactic bacteria of the iron oxide type are associated with the a subgroup of the Proteobacteria in the domain Bacteria. In contrast, uncultured magnetotactic bacteria of the iron sulfide type are specifically related to the dissimilatory sulfate-reducing bacteria within the δ subdivision of the Proteobacteria. These findings indicate a polyphyletic origin for magnetotactic bacteria and suggest that magnetotaxis based on iron oxides and iron sulfides evolved independently.

Electron Microscopy Study of Magnetosomes in a Cultured Coccoid Magnetotactic Bacterium

Intracellular magnetite (Fe3O4) crystals produced by the magnetotactic bacterium MC-1 were analysed by transmission electron microscopy (TEM). Strain MC-1 represents the first-reported isolation of a coccoid magnetotactic bacterium in axenic culture. The magnetosomes of this bacterium displayed a pseudo-hexagonal prismatic habit, were elongated along <111> the crystallographic direction, and were truncated by {111}, {100} and {110} faces. The presence of {111} truncations represents a modification of the magnetosome morphology previously determined for those in other coccoid bacteria. Study of immature crystals produced by strain MC-1 showed that the crystal morphology was controlled even at early stages of development. Changes in the culture media affected both the number and shape of the bacterial magnetite crystals. Cells grown in an acetate-containing medium contained on average more crystals than those in cells grown in a sulphide-containing medium. Crystals synthesized in the acetate-grown cells tended to be less truncated than those in the sulphide-grown cells. No iron sulphide minerals, such as greigite, were observed in cells grown in the presence of sulphide.

Fe3O4 precipitation in magnetotactic bacteria

Abstract Using Mossbauer resonance spectroscopy of 57Fe, we have determined the nature and distribution of major iron compounds in the magnetotactic bacterium Aquaspirillum magnetotacticum. In addition to magnetite (Fe3O4), cells contained a low-density hydrous ferric oxide, a high-density hydrous ferric oxide (ferrihydrite), and ferrous iron. Analysis at different temperatures of whole cells harvested early and late in growth, of mutant cells unable to synthesize magnetite, and of cell fractions enriched in 57Fe indicated that Fe3O4 precipitation resulted from partial reduction of the high-density hydrous ferric oxide precursor.