Extracellular Magnetite Research Articles

Interpretation of Anhysteretic Remanent Magnetization Carriers in Magnetofossil‐Rich Marine Sediments

AbstractThe anhysteretic remanent magnetization (ARM) is an important magnetic parameter for quantifying the concentration of “fine”, mostly sub‐micron ferrimagnetic particles in rocks and sediments. A sound understanding of ARM carriers is needed to interpret magnetic and environmental information in sedimentary archives. This is often not achieved for marine sediments, which routinely contain several magnetic mineral components. Here, we analyze marine sediment records over different timescales for four sediment cores from the Eastern Pacific Ocean (Hole 1218A), the Antarctic margin (core P4‐1), the Arctic Ocean (core ARC5‐ICE4), and the South China Sea (core L07), using coercivity spectra analyses of ARM, first‐order reversal curve principal component analysis (FORC‐PCA), transmission electron microscopy (TEM), and unmixing of isothermal remanent magnetization (IRM) curves. By combining rock magnetic and TEM results, we find that the ARM is mainly carried by non‐interacting single domain (SD) biogenic magnetite (magnetofossils) in the studied sediments over all timescales. Low‐coercivity magnetic particles (detrital and fine‐grained extracellular magnetite) also contribute to the bulk ARM. Variable magnetofossil chain structures are detected and have a significant influence on ARM data interpretation. Quantitative FORC‐PCA endmember analyses based on quantile contours and coercivity distributions provide valuable information on the nature of endmembers and improve ARM data interpretation. We provide an integrated strategy to help reduce interpretational ambiguities related to ARM in future studies.

Geobacter Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms

ABSTRACTCytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence for these proposed DIET mechanisms has been lacking. To investigate these possibilities further, we constructed Geobacter metallireducens strain Aro-5, in which the wild-type pilin gene was replaced with the aro-5 pilin gene that was previously shown to yield poorly conductive pili in Geobacter sulfurreducens strain Aro-5. G. metallireducens strain Aro-5 did not reduce Fe(III) oxide and produced only low current densities, phenotypes consistent with expression of poorly conductive pili. Like G. sulfurreducens strain Aro-5, G. metallireducens strain Aro-5 displayed abundant outer surface cytochromes. Cocultures initiated with wild-type G. metallireducens as the electron-donating strain and G. sulfurreducens strain Aro-5 as the electron-accepting strain grew via DIET. However, G. metallireducens Aro-5/G. sulfurreducens wild-type cocultures did not. Cocultures initiated with the Aro-5 strains of both species grew only when amended with granular activated carbon (GAC), a conductive material known to be a conduit for DIET. Magnetite could not substitute for GAC. The inability of the two Aro-5 strains to adapt for DIET in the absence of GAC suggests that there are physical constraints on establishing DIET solely through cytochrome-to-cytochrome electron transfer or along chains of magnetite. The finding that DIET is possible with electron-accepting partners that lack highly conductive pili greatly expands the range of potential electron-accepting partners that might participate in DIET.

In Vitro Investigation of the Effect of Intracellular and Extracellular Magnetite Nanoparticles Subjected to Alternating Magnetic Field on MCF‐7 Human Breast Cancer Cells

AbstractTo evaluate the efficiency with which intra‐ and extracellular magnetite nanoparticles (MNPs) induce cell death under an alternating magnetic field (AMF), we comparatively investigated two systems consisting of MCF‐7 human breast cancer cells and MNPs: one is a “simply‐added” system, which is essentially a simple mixture of cells and extracellular MNPs, and the other is a “pre‐cultivated” system that contains both intra‐ and extracellular MNPs. We also evaluated the effect of heating by thermostatic water bath (WB) on cell death in both systems. The degree of cell death was greater under heating with MNPs subjected to AMF than in the WB‐heating in both systems. At higher doses of MNPs, the degree of cell death was greater in the “pre‐cultivated” system than in the “simply‐added” system using both heating methods. The cellular uptake of MNPs induced slight cell damage and caused a high degree of cell death at higher temperatures. A significant decrease in cell viability was observed in the presence of internalized MNPs under the AMF and was suggested to be a result of the combined effect of intracellular heating and cellular damage by MNPs.

Pond sediment magnetite grains show a distinctive microbial community.

Formation of magnetite in anaerobic sediments is thought to be enhanced by the activities of iron-reducing bacteria. Geobacter has been implicated as playing a major role, as in culture its cells are often associated with extracellular magnetite grains. We studied the bacterial community associated with magnetite grains in sediment of a freshwater pond in South Korea. Magnetite was isolated from the sediment using a magnet. The magnetite-depleted fraction of sediment was also taken for comparison. DNA was extracted from each set of samples, followed by PCR for 16S bacterial ribosomal RNA (rRNA) gene and HiSeq sequencing. The bacterial communities of the magnetite-enriched and magnetite-depleted fractions were significantly different. The enrichment of three abundant operational taxonomic units (OTUs) suggests that they may either be dependent upon the magnetite grain environment or may be playing a role in magnetite formation. The most abundant OTU in magnetite-enriched fractions was Geobacter, bolstering the case that this genus is important in magnetite formation in natural systems. Other major OTUs strongly associated with the magnetite-enriched fraction, rather than the magnetite-depleted fraction, include a Sulfuricella and a novel member of the Betaproteobacteria. The existence of distinct bacterial communities associated with particular mineral grain types may also be an example of niche separation and coexistence in sediments and soils, which cannot usually be detected due to difficulties in separating and concentrating minerals.

Formation of single domain magnetite by green rust oxidation promoted by microbial anaerobic nitrate-dependent iron oxidation

Biomineralization of magnetite is a central geomicrobiological process that might have played a primordial role over Earth’s history, possibly leaving traces of life in the geological record or controlling trace metal(loid)s and organic pollutants mobility in modern environments. Magnetite biomineralization has been attributed to two main microbial pathways to date (namely magnetotactic bacteria and dissimilatory iron-reducing bacteria). Here, we uncover a new route of magnetite biomineralization involving the anaerobic nitrate-reducing iron(II) oxidizing bacterium Acidovorax sp. strain BoFeN1. Using transmission electron microscopy, scanning transmission X-ray microscopy, transmission Mössbauer spectroscopy and rock magnetic analyses, this strain is shown to promote the transformation of hydroxychloride green rust in equilibrium with dissolved Fe(II) to (1) periplasmic lepidocrocite (γ-FeOOH) and (2) extracellular magnetite, thus leading to strong redox heterogeneities at the nanometer scale. On the one hand, lepidocrocite was associated with protein moieties and exhibited an anisotropic texture, with the elongated axis parallel to the cell wall. On the other hand, magnetite crystals exhibited grain sizes and magnetic properties consistent with stable single domain particles. By comparison, abiotic controls led to a very slow (4months vs. 2days in BoFeN1 cultures) and incomplete oxidation of hydroxychloride green rust towards magnetite. As this abiotic magnetite exhibited the same size and magnetic properties (stable single domain particles) as magnetite produced in BoFeN1 cultures, only the co-occurrence of textured Fe(III)-oxides and magnetite, associated with the persistence of organic carbon molecules, might constitute valuable biosignatures to be looked for in the geological record. Our results furthermore contribute to a more complex picture of Fe redox cycling in the environment, providing an additional process of Fe(II)-bearing phase biomineralization that is not specific of Fe bio-reduction, but can also result from Fe bio-oxidation.

Sources of fine-grained magnetic minerals in sediments: a problem revisited

Progress in the discrimination of fine-grained magnetic minerals in sediments and sediment sources using measurements of magnetic susceptibility at two frequencies and of magnetic remanence generated by a combination of direct and alternating currents is summarized. The former measurements yield values for low field and frequency-dependent susceptibility (χlf and χfd, respectively). The latter generate an Anhysteretic Remanent Magnetisation (ARM) that, when normalized to the DC bias field, can be represented as the susceptibility of ARM (χARM). Using quotients derived from χlf, χfd and χ ARM to generate bi-logarithmic plots, it is possible to discriminate between assemblages dominated by magnetic minerals formed through pedogenesis and those arising from the presence of magnetotactic bacteria that use chains of magnetic particles to seek optimum environments in surface sediments. Sediments to which both types of magnetic mineral contribute occupy positions between the envelopes of values typical of soil-derived and magnetosome-derived assemblages. Fire also appears to give rise to a distinctive envelope of values indicative of smaller magnetic grain sizes, whilst the signature of extracellular magnetite is indicative of the finest grain sizes here recorded.

An integrated approach for determining the origin of magnetite nanoparticles

The criteria to assess the origin of magnetite are of prime importance because of their significance as biomarkers for extraterrestrial life and paleoenvironmental indicators. It is still unclear if morphology and magnetic properties of crystals do quantitatively allow differentiating abiotic from biotic magnetite crystals of nanometer size. In this study, inorganic magnetite nanocrystals synthesized under controlled experimental aqueous conditions are compared with biogenic magnetite of similar size and morphology formed by magnetotactic (intracellular magnetite) and other (extracellular magnetite) bacteria. Structural properties such as oxygen isotope fractionations and crystal size distributions were explored. Not surprisingly, none of the single properties are able to differentiate inorganic crystals from those having a bacterial origin, either specifically extracellular or specifically intracellular. However, oxygen isotope fractionation allows the differentiation between abiotic and biotic magnetite when the temperature of formation is known and when it does not fall into a crossing region (35 ≤ T (°C) ≤ 55) while crystal size distributions discriminate inorganic from intracellular magnetite. Therefore, a combination of these two properties may be a successful tool for an accurate determination of a reliable biogenicity criterion.

Formation of tabular single-domain magnetite induced by Geobacter metallireducens GS-15.

Distinct morphological characteristics of magnetite formed intracellularly by magnetic bacteria (magnetosome) are invoked as compelling evidence for biological activity on Earth and possibly on Mars. Crystals of magnetite produced extracellularly by a variety of bacteria including Geobacter metallireducens GS-15, thermophilic bacteria, and psychrotolerant bacteria are, however, traditionally not thought to have nearly as distinct morphologies. The size and shape of extracellular magnetite depend on the culture conditions and type of bacteria. Under typical CO(2)-rich culture conditions, GS-15 is known to produce superparamagnetic magnetite (crystal diameters of approximately <30 nm). In the current study, we were able to produce a unique form of tabular, single-domain magnetite under nontraditional (low-CO(2)) culture conditions. This magnetite has a distinct crystal habit and magnetic properties. This magnetite could be used as a biosignature to recognize ancient biological activities in terrestrial and extraterrestrial environments and also may be a major carrier of the magnetization in natural sediments.

Reduction of Fe(III), Mn(IV), and toxic metals at 100 degrees C by Pyrobaculum islandicum.

It has recently been noted that a diversity of hyperthermophilic microorganisms have the ability to reduce Fe(III) with hydrogen as the electron donor, but the reduction of Fe(III) or other metals by these organisms has not been previously examined in detail. When Pyrobaculum islandicum was grown at 100 degrees C in a medium with hydrogen as the electron donor and Fe(III)-citrate as the electron acceptor, the increase in cell numbers of P. islandicum per mole of Fe(III) reduced was found to be ca. 10-fold higher than previously reported. Poorly crystalline Fe(III) oxide could also serve as the electron acceptor for growth on hydrogen. The stoichiometry of hydrogen uptake and Fe(III) oxide reduction was consistent with the oxidation of 1 mol of hydrogen resulting in the reduction of 2 mol of Fe(III). The poorly crystalline Fe(III) oxide was reduced to extracellular magnetite. P. islandicum could not effectively reduce the crystalline Fe(III) oxide minerals goethite and hematite. In addition to using hydrogen as an electron donor for Fe(III) reduction, P. islandicum grew via Fe(III) reduction in media in which peptone and yeast extract served as potential electron donors. The closely related species P. aerophilum grew via Fe(III) reduction in a similar complex medium. Cell suspensions of P. islandicum reduced the following metals with hydrogen as the electron donor: U(VI), Tc(VII), Cr(VI), Co(III), and Mn(IV). The reduction of these metals was dependent upon the presence of cells and hydrogen. The metalloids arsenate and selenate were not reduced. U(VI) was reduced to the insoluble U(IV) mineral uraninite, which was extracellular. Tc(VII) was reduced to insoluble Tc(IV) or Tc(V). Cr(VI) was reduced to the less toxic, less soluble Cr(III). Co(III) was reduced to Co(II). Mn(IV) was reduced to Mn(II) with the formation of manganese carbonate. These results demonstrate that biological reduction may contribute to the speciation of metals in hydrothermal environments and could account for such phenomena as magnetite accumulation and the formation of uranium deposits at ca. 100 degrees C. Reduction of toxic metals with hyperthermophilic microorganisms or their enzymes might be applied to the remediation of metal-contaminated waters or waste streams.

Possible evidence for dissimilatory bacterial magnetite dominating the magnetic properties of recent lake sediments

Rock magnetic measurements, including low temperature susceptibility and Curie Temperature experiments, show that the most recent sediments from the Bay of Vidy, close to Lausanne on the north shore of Lake Geneva, Switzerland, are rich in superparamagnetic magnetite. The 137Cs dated increase in magnetite concentration coincides with the beginning of sewage de-phosphatization by the addition of iron chloride. Extracts of fine-grained magnetite, imaged by transmission electron microscopy, form amorphous masses visually comparable to those detected as the product of extracellular magnetite production by bacteria. This is the first indication that extracellular, dissimilatory magnetite may survive and make a dominant contribution to the magnetic properties of sediments. Final confirmation of the bacterial origin of the magnetite will depend on rRNA sequencing.

Fe(III) as an electron acceptor for H2 oxidation in thermophilic anaerobic enrichment cultures from geothermal areas.

Six sustainable enrichment cultures of thermophilic H2-oxidizing microorganisms utilizing Fe(III) as an electron acceptor were obtained from geothermally heated environments located on two continents (America, Eurasia) and on islands in the Northern (Iceland) and Southern (Fiji) hemispheres, demonstrating the wide distribution of these microorganisms. The main products of amorphic Fe(III) oxide reduction were magnetite and siderite. The observed temperature range for Fe(III) reduction in growing cultures was from 55 degrees C to 87 degrees C, extending the known limits for growth of Fe(III)-reducing microorganisms producing extracellular magnetite to nearly 90 degrees C.

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.

Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism

The potential contribution of microbial metabolism to the magnetization of sediments has only recently been recognized. In the presence of oxygen, magnetotactic bacteria can form intracellular chains of magnetite while using oxygen or nitrate as the terminal electron acceptor for metabolism1. The production of ultrafine-grained magnetite by magnetotactic bacteria in surficial aerobic sediments may contribute significantly to the natural remanent magnetism of sediments2–4. However, recent studies on iron reduction in anaerobic sediments suggested that bacteria can also generate magnetite in the absence of oxygen5. We report here on a sediment organism, designated GS-15, which produces copious quantities of ultrafine-grained magnetite under anaerobic conditions. GS-15 is not magnetotactic, but reduces amorphic ferric oxide to extracellular magnetite during the reduction of ferric iron as the terminal electron acceptor for organic matter oxidation. This novel metabolism may be the mechanism for the formation of ultrafine-grained magnetite in anaerobic sediments, and couldaccount for the accumulation of magnetite in ancient iron formations and hydrocarbon deposits.