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Magnetotactic bacteria (MTB) are diverse prokaryotes that produce magnetic nanocrystals within intracellular membranes (magnetosomes). Here, we present a large-scale analysis of diversity and magnetosome biomineralization in modern magnetotactic cocci, which are the most abundant MTB morphotypes in nature. Nineteen novel magnetotactic cocci species are identified phylogenetically and structurally at the single-cell level. Phylogenetic analysis demonstrates that the cocci cluster into an independent branch from other Alphaproteobacteria MTB, that is, within the Etaproteobacteria class in the Proteobacteria phylum. Statistical analysis reveals species-specific biomineralization of magnetosomal magnetite morphologies. This further confirms that magnetosome biomineralization is controlled strictly by the MTB cell and differs among species or strains. The post-mortem remains of MTB are often preserved as magnetofossils within sediments or sedimentary rocks, yet paleobiological and geological interpretation of their fossil record remains challenging. Our results indicate that magnetofossil morphology could be a promising proxy for retrieving paleobiological information about ancient MTB.

金沢大学理工研究域地球社会基盤学系, Single-domain magnetite particles exhibit minimum susceptibility along their elongation, resulting in so-called inverse fabric of the anisotropy of magnetic susceptibility (AMS). We report the discovery of inverse AMS fabrics from pelagic clay recovered by a ∼12m long piston core from the western North Pacific. A previous study identified fossil single-domain magnetite produced by magnetotactic bacteria (magnetofossils) as the dominant ferrimagnetic mineral in the sediment. The inverse AMS fabrics were found in a ∼2m zone. The ∼6 and ∼4m of sediment above and below this zone showed normal, horizontal AMS fabrics. Rock magnetic data and ferromagnetic resonance spectroscopy indicated that magnetofossils account for most of the mean susceptibility regardless of normal or inverse AMS. This was explained by the mixing models where the inverse fabric from magnetofossils is nearly balanced by the normal fabrics of terrigenous minerals. The corrected degree of AMS carried by magnetofossils in the sediment was estimated to be ∼1.01, which is comparable to that of typical pelagic sediment at shallow depth. On the other hand, terrigenous minerals in the sediment were estimated to have higher degree of anisotropy, possibly reflecting burial and subsequent erosion of >80m of sediment, which was also suggested by a subbottom acoustic stratigraphy. This suggests that inverse AMS fabrics due to magnetofossils may be widespread in pelagic clay without strong compaction. ©2019. American Geophysical Union. All Rights Reserved.

21 pages; International audience; Magnetotactic bacteria (MTB) intracellularly precipitate magnetite (Fe3O4) crystals that can be preserved in the geological record. When MTB die, the so-called magnetofossils constitute valuable proxies for paleoenvironmental reconstructions and are suspected to represent some of the oldest traces of biomineralization on Earth. Yet, the biogenicity of putative magnetofossils found in ancient terrestrial and extra-terrestrial samples is still largely debated and their significance for past climate still holds uncertainties. Here we studied a sedimentary sequence from the Indian Ocean (ODP Hole 711A) recording the Middle Eocene Climatic Optimum (MECO) through which a magnetofossil-rich interval was deposited. We investigated for the first time the potential of Fe isotopes as a biosignature in magnetofossils and thoroughly describe MECO related paleoenvironmental disruptions based on major and trace element concentrations. Bulk sediment Fe isotopes showed limited variations, with δ56Fe around −0.13 ± 0.04‰ (n = 24), linked to detrital iron rather than MTB activity. Hence, a sequential chemical extraction protocol was applied to determine the specific composition of magnetite. We discuss analytical biases related to this protocol (i.e. partial phyllosilicate and Mn-oxide leaching) and apply corrections to the data. Outside the magnetofossil-rich interval, Fe isotope compositions of oxides (mainly biotic and/or abiotic magnetites and possibly Fe coprecipitated with Mn-oxides) display a small range averaging −0.54 ± 0.05‰, and are interpreted as reflecting dominantly hydrothermal contribution, a conclusion also supported by prominent Eu anomaly. In contrast, the magnetofossil-rich interval shows larger δ56Fe variability in oxides, from −0.12 to −0.94‰, decreasing upwards in the stratigraphic section. This interval likely records enhanced Fe supply from atmospheric fallout, increase in biological productivity (illustrated by increased Ba accumulation rate) and subsequent development of ferruginous conditions in the sediment porewater. Covariations of Fe isotope compositions and Mn/Fe ratios can be explained by a vertical migration of a redox front and associated diagenetic modifications. Precipitation of barite (BaSO4) in the sediments after organic matter decay probably favored the preservation of magnetofossils by decreasing SO42- concentration in porewaters and subsequent H2S production, which usually dissolve magnetite in the sulfidic zone. Finally, we model the evolution of porewater fluid and estimate Fe isotope fractionation between magnetofossils and fluid to Δ56Femag-Fe(II)aq = 0.1–0.3‰, a value significantly different from abiotic magnetite fractionation (~1.5‰). Contrasting with recent results on MTB laboratory culture, no mass independent fractionation of Fe isotopes was observed in the present study. Nevertheless, the diverse geochemical proxies presented here provide important constraints on paleoclimate and magnetofossil biogenicity evaluation.

Magnetotactic bacteria (MTB) play an important role in biogeochemical cycles of iron and remanent magnetization acquisition of sediments. It is generally considered that magnetite-producing MTB prefer chemical conditions in the oxic-anoxic transition zone (OATZ). We studied the distribution of fossil MTB magnetite (magnetofossils) and microbes phylogenetically related to MTB within deep-sea surface sediments across the OATZ. Transmission electron microscope (TEM) observations and rock-magnetic proxies show that magnetofossils commonly occur both within the OATZ and above it, even at the top of surface oxidized layers, and that the proportion of magnetofossils with a teardrop morphology increases within the OATZ. Consistent results were obtained from the pyrosequencing of 16S rRNA gene fragments. Operational taxonomic units (OTUs) related to Nitrospirae and OP3 MTB, which produce teardrop-shape magnetosomes, were detected only within the OATZ, whereas OTUs related to alphaproteobacterial MTB, which produce equant or elongated magnetite particles, were distributed above the OATZ. These results suggest that magnetofossil morphology can be used to detect past OATZs, and that some MTB lineages can occur ubiquitously in marine sediments rather than being limited within the OATZ. Our results imply that the timing of remanent magnetization acquisition may depend on the inhabiting MTB lineages.

Understanding marine environmental change and associated biological turnover across the Palaeocene–Eocene Thermal Maximum (PETM; ~56 Ma)—the most pronounced Cenozoic short-term global warming event—is important because of the potential role of the ocean in atmospheric CO2 drawdown, yet proxies for tracing marine productivity and oxygenation across the PETM are limited and results remain controversial. Here we show that a high-resolution record of South Atlantic Ocean bottom water oxygenation can be extracted from exceptionally preserved magnetofossils—the bioinorganic magnetite nanocrystals produced by magnetotactic bacteria (MTB) using a new multiscale environmental magnetic approach. Our results suggest that a transient MTB bloom occurred due to increased nutrient supply. Bottom water oxygenation decreased gradually from the onset to the peak PETM. These observations provide a record of microbial response to the PETM and establish the value of magnetofossils as palaeoenvironmental indicators., Understanding the response of marine productivity and CO2 drawdown to past warming events can provide important insights into the future. Here, the authors use bacterial magnetite nanoparticle fossils to reconstruct nutrient supply and marine deoxygenation during the Palaeocene–Eocene Thermal Maximum.

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.

Redox variations govern a multitude of key geochemical and microbiological processes within lacustrine and marine systems, yet the interpretation of these geological archives can be limited because redox-sensitive microorganisms leave behind sparse fossil evidence. Here, we assess a biologically controlled magnetic proxy through investigation of a well-constrained sedimentary record covering a perturbation of redox-conditions driven by a complete trophic cycle in Lake Constance. Ferromagnetic resonance spectroscopy of sediments reveals strong uniaxial anisotropy, indicative of single-domain magnetite particles in intact or fragmentary chain arrangements, which are an unambiguous trait of magnetotactic bacteria (MTB) and their magnetofossil remains. We show that biogenic magnetite formed intra-cellularly in MTB faithfully records changing redox-conditions at or close to the sediment water-interface. Biogenic magnetite within sedimentary records points to the proliferation of MTB parallel to a decline in water column dissolved oxygen and the formation of sulfidic surface sediments in Lake Constance associated with an episode of eutrophication (1955–1991). We conclude that magnetofossils may serve as a sensitive geological proxy to reconstruct dynamic redox-changes along the sediment-water interface and bottom waters., Earth and Planetary Science Letters, 545, ISSN:0012-821X, ISSN:1385-013X

Redox variations govern a multitude of key geochemical and microbiological processes within lacustrine and marine systems, yet the interpretation of these geological archives can be limited because redox-sensitive microorganisms leave behind sparse fossil evidence. Here, we assess a biologically controlled magnetic proxy through investigation of a well-constrained sedimentary record covering a perturbation of redox-conditions driven by a complete trophic cycle in Lake Constance. Ferromagnetic resonance spectroscopy of sediments reveals strong uniaxial anisotropy, indicative of single-domain magnetite particles in intact or fragmentary chain arrangements, which are an unambiguous trait of magnetotactic bacteria (MTB) and their magnetofossil remains. We show that biogenic magnetite formed intra-cellularly in MTB faithfully records changing redox-conditions at or close to the sediment water-interface. Biogenic magnetite within sedimentary records points to the proliferation of MTB parallel to a decline in water column dissolved oxygen and the formation of sulfidic surface sediments in Lake Constance associated with an episode of eutrophication (1955–1991). We conclude that magnetofossils may serve as a sensitive geological proxy to reconstruct dynamic redox-changes along the sediment-water interface and bottom waters.

The oriented chains of nanoscale Fe-oxide particles produced by magnetotactic bacteria are a striking example of biomineralization. Several distinguishing features of magnetite particles that comprise bacterial magnetosomes have been proposed to collectively constitute a biosignature of magnetotactic bacteria (Thomas-Keprta et al., 2001). These features include high crystallinity, chemical purity, a single-domain magnetic structure, well-defined crystal morphology, and arrangement of particles in chain structures. Here, we show that magnetite derived from the inorganic breakdown of nanocrystalline goethite exhibits magnetic properties and morphologies remarkably similar to those of biogenic magnetite from magnetosomes. During heating in reducing conditions, oriented nanogoethite aggregates undergo dehydroxylation and transform into stoichiometric magnetite. We demonstrate that highly crystalline single-domain magnetite with euhedral grain morphologies produced abiogenically from goethite meets several of the biogenicity criteria commonly used for the identification of magnetofossils. Furthermore, the suboxic conditions necessary for magnetofossil preservation in sediments are conducive to the reductive alteration of nanogoethite, as well as the preservation of detrital magnetite originally formed from goethite. The findings of this study have potential implications for the identification of biogenic magnetite, particularly in older sediments where diagenesis commonly disrupts the chain structure of magnetosomes. Our results indicate that isolated magnetofossils cannot be positively distinguished from inorganic magnetite on the basis of their magnetic properties and morphology, and that intact chain structures remain the only reliable distinguishing feature of fossil magnetosomes., This work was supported by the “Agence nationale de la recherche” (France) under project 2010-BLAN-604-01. Dennis Kent and Joshua Feinberg are thanked for their constructive reviews. This is IPGP contribution 3826., Final draft post-review

[1] The widespread occurrence of magnetotactic bacteria (MTB) in several types of marine and freshwater sediment, and the role of fossil magnetosomes (magnetofossils) as main remanent magnetization carriers therein, has important paleomagnetic and paleoenvironmental implications. Despite numerous studies on MTB biology and on magnetofossil preservation in geological records, no detailed information is yet available on how magnetotaxis (i.e., the ability to navigate along magnetic field lines) is performed in sedimentary environments, and on how magnetofossils possibly record the Earth magnetic field. We provide for the first time experimental evidence for these processes. MTB living in sediment are poorly aligned with the geomagnetic field, contrary to what is observed in water. This can explain the seemingly excessive magnetic moment of most MTB. The observed alignment is sufficient for supporting magnetotaxis across the typical thickness of chemical gradients. Experiments with magnetofossil-rich sediment suggest that a natural remanent magnetization (NRM) is acquired by magnetofossils in the so-called benthic mixed layer, where natural MTB populations usually occur. The acquired NRM is proportional to the applied field at least up to ∼160 µT, and its intensity is compatible with values observed in nature for same sediment types. Therefore, if fossil magnetosome chains are not subjected to further alteration by early diagenetic processes, they can provide useful relative paleointensities. We propose a preliminary model to explain early stages of magnetofossil NRM acquisition as the result of a dynamic equilibrium between magnetic torques and randomizing forces due to sediment mixing.

Pelagic carbonates are deposited far from continents, usually at water depths of 3000–6000 m, at rates below 10 cm/kyr, and are a globally important sediment type. Recent advances, with recognition of widespread preservation of biogenic magnetite (the inorganic remains of magnetotactic bacteria), have fundamentally changed our understanding of the magnetic properties of pelagic carbonates. We review evidence for the magnetic minerals typically preserved in pelagic carbonates, the effects of magnetic mineral diagenesis on paleomagnetic and environmental magnetic records of pelagic carbonates, and what magnetic properties can tell us about the open-ocean environments in which pelagic carbonates are deposited. We also discuss briefly late diagenetic remagnetisations recorded by some carbonates. Despite recent advances in our knowledge of these phenomena, much remains undiscovered. We are only at early stages of understanding how biogenic magnetite gives rise to paleomagnetic signals in sediments and whether it carries a poorly understood biogeochemical remanent magnetisation. Recently developed techniques have potential for testing how different magnetotactic bacterial species, which produce different magnetite morphologies, respond to changing nutrient and oxygenation conditions. Future work needs to test whether it is possible to develop proxies for ancient nutrient conditions from well-calibrated modern magnetotactic bacterial occurrences. A tantalizing link between giant magnetofossils and Paleogene hyperthermal events needs to be tested; much remains to be learned about the relationship between climate and the organisms that biomineralised these large and novel magnetite morphologies. Rather than being a well-worn subject that has been studied for over 60 years, the magnetic properties of pelagic carbonates hold many secrets that await discovery.

Mineral magnetic and ferromagnetic resonance (FMR) measurements made on the sediments from Lake Ely, Pennsylvania reveal the presence of magnetotactic bacteria magnetofossils. Saturation isothermal remanent magnetization (SIRM) data from a 1.25 m long piston core taken from the deepest part of the lake show a large intensity decrease at depths between 30 and 75 cm in the sediment column most likely the result of reductive diagenesis. Modeling of isothermal remanent magnetization (IRM) and anhysteretic remanent magnetization (ARM) acquisition data indicates the presence of biogenic soft (BS) and biogenic hard (BH) magnetosome coercivity components, even at depths in the core greatly affected by reductive diagenesis. First-order reversal curve distribution diagrams for two samples support this interpretation. Modeling of the FMR data also indicates the presence of the BS and BH magnetosome coercivity components, but the relative importance of the two components is opposite to that seen for the IRM and ARM acquisition modeling. A correlation between SIRM variations and local rainfall recorded over the past 70 years suggests that magnetofossil concentrations recorded paleo-rainfall variations in the most recent lake sediments. Multi-taper method spectral analysis of SIRM variations in the piston core, tied to time by varve counting from 1600 common era (CE) to 1128 before CE, show centennial scale periodicities similar to those observed in spectral analysis of a 230 year long historical rainfall record for the northeastern US reconstructed to Philadelphia, PA. This result indicates that enough magnetofossils can survive reductive diagenesis to retain a record of paleorainfall variations, suggesting that they can be a powerful paleoclimate proxy.

Magnetotactic bacteria (MTB) produce chains of intracellular magnetite and/or greigite crystals and respond to an ambient magnetic field. MTB are considered to be microaerophilic to anaerobic organisms that live at and below the oxic-anoxic transition zone of aquatic environments. On the basis of rock magnetic analyses, including first-order reversal curve diagrams and isothermal remanent magnetization component analyses, along with transmission electron microscopy, we demonstrate that bacterial magnetites (magnetofossils) dominate magnetic mineral assemblages throughout a 76 m thickness of red clay at Integrated Ocean Drilling Program Site U1365 in the South Pacific Gyre, as well as in subsurface red clay of the North Pacific Gyre, where the sediment column contains abundant dissolved oxygen and no oxic-anoxic transition zone exists. This implies that MTB inhabit red clay; this conflicts with widespread interpretations of MTB ecology, namely that they are microaerophilic, requiring low levels of oxygen to grow and produce magnetite, and that magnetotaxis is used to help them find optimal positions in a strong vertical chemical gradient. Most magnetofossils in the red clay have cubo-octahedral morphology. This supports the notion that magnetofossil morphology can be a paleoenvironmental indicator; the proportion of elongated magnetofossils increases in less oxic environments. Our results also have implications for red-clay paleomagnetism in that magnetofossils may cause much-delayed remanence acquisition if MTB can live at decimeter depths within red clay.

article i nfo Article history: Magnetotactic bacteria intracellularly biomineralize magnetite of an ideal grain size for recording palaeomagnetic signals. However, bacterial magnetite has only been reported in a few pre-Quaternary records because progressive burial into anoxic diagenetic environments causes its dissolution. Deep-sea carbonate sequences provide optimal environments for preserving bacterial magnetite due to low rates of organic carbon burial and expanded pore-water redox zonations. Such sequences often do not become anoxic for tens to hundreds of metres below the seafloor. Nevertheless, the biogeochemical factors that control magnetotactic bacterial populations in such settings are not well known. We document the preservation of bacterial magnetite, which dominates the palaeomagnetic signal throughout Eocene pelagic carbonates from the southern Kerguelen Plateau, Southern Ocean. We provide evidence that iron fertilization, associated with increased aeolian dust flux, resulted in surface water eutrophication in the late Eocene that controlled bacterial magnetite abundance via export of organic carbon to the seafloor. Increased flux of aeolian iron- bearing phases also delivered iron to the seafloor, some of which became bioavailable through iron reduction. Our results suggest that magnetotactic bacterial populations in pelagic settings depend crucially on particulate iron and organic carbon delivery to the seafloor.

Magnetotactic bacteria contain chains of magnetically interacting crystals (magnetosome crystals), which they use for navigation (magnetotaxis). To improve magnetotaxis efficiency, the magnetosome crystals (usually magnetite or greigite in composition) should be magnetically stable single-domain (SSD) particles. Smaller single-domain particles become magnetically unstable owing to thermal fluctuations and are termed superparamagnetic (SP). Previous calculations for the SSD/SP threshold size or blocking volume did not include the contribution of magnetic interactions. In this study, the blocking volume has been calculated as a function of grain elongation and separation for chains of identical magnetite grains. The inclusion of magnetic interactions was found to decrease the blocking volume, thereby increasing the range of SSD behaviour. Combining the results with previously published calculations for the SSD to multidomain threshold size in chains of magnetite reveals that interactions significantly increase the SSD range. We argue that chains of interacting magnetosome crystals found in magnetotactic bacteria have used this effect to improve magnetotaxis.

Magnetotactic bacteria, which most commonly live within the oxic-anoxic transition zone (OATZ) of aquatic environments, produce intracellular crystals of magnetic minerals, specifically magnetite or greigite. The crystals cause the bacteria to orient themselves passively with respect to the geomagnetic field and thereby facilitate the bacteria’s search for optimal conditions within the sharp chemical gradients of the OATZ. The bacteria may also gain energy from the redox cycling of their crystals. Because magnetotactic bacteria benefit from their magnetic moments, natural selection has promoted the development of traits that increase the efficiency with which the intracellular crystals impart magnetic moments to cells. These traits also allow crystals produced by magnetotactic bacteria (called magnetofossils when preserved in sediments) to be distinguished from abiogenic particles and particles produced as extracellular byproducts of bacterial metabolism. Magnetofossils are recognizable based on their narrow size and shape distributions, distinctive morphologies with blunt crystal edges, chain arrangement, chemical purity, and crystallographic perfection. This article presents a scheme for rating magnetofossil robustness based on these traits. The magnetofossil record extends robustly to the Cretaceous and with lesser certainty to the late Archean. Because magnetotactic bacteria predominantly live in the OATZ, the abundance and character of their fossils can reflect environmental changes that alter the chemical stratification of sediments and the water column. The magnetofossil record therefore provides an underutilized archive of paleoenvironmental information. Several studies have demonstrated a relationship between magnetofossil abundance and glacial/interglacial cycles, likely mediated by changes in pore water oxygen levels. More speculatively, a better-developed magnetofossil record might provide constraints on the long-term evolution of marine redox stratification. More work in modern and ancient settings is necessary to explicate the mechanisms linking the abundance and character of magnetofossils to ancient biogeochemistry.

Magnetotactic bacteria produce intracellular crystals of magnetite or greigite, the properties of which have been shaped by evolution to maximize the magnetic moment per atom of iron. Intracellular bacterial magnetite therefore possesses traits amenable to detection by physical techniques: typically, narrow size and shape distributions, single-domain size and arrangement in linear chains, and often crystal elongation. Past strategies for searching for bacterial magnetofossils using physical techniques have focused on identifying samples containing significant amounts of single domain magnetite or with narrow coercivity distributions. Searching for additional of traits would, however, increase the likelihood that candidate magnetofossils are truly of biological origin. Ferromagnetic resonance spectroscopy (FMR) is in theory capable of detecting the distinctive magnetic anisotropy produced by chain arrangement and crystal elongation. Here we present analyses of intact and lysed magnetotactic bacteria, dilutions of synthetic magnetite, and sedimentary samples of modern carbonates from the Great Bahama Bank, Oligocene–Miocene deep-sea muds from the South Atlantic, and Pleistocene lacustrine deposits from Mono Basin, California. We demonstrate that FMR can distinguish between intact bacterial magnetite chains, collapsed chains, and linear strings of magnetite formed by physical processes. We also show that sediments in which the magnetization is likely carried by bacterial magnetite have FMR spectra resembling those of intact or altered bacterial magnetite chains.

Magnetotactic bacteria precipitate intracellular crystals of single-domain magnetite (Fe3O4) and/or greigite (Fe3S4), which have often been implicated in carrying the natural remanent magnetization (NRM) of freshwater and marine sediments. In vivo, the magnetic crystals are usually aligned in chains such that their moments add together, generating net cellular moments high enough to rotate the cells passively to align with the geomagnetic field. A magnetostatic/biophysical analysis demonstrates that this arrangement is out of dynamic equilibrium and would collapse spontaneously without a support mechanism. Past rock magnetic analyses of shallow water marine carbonates suggest that partial collapse does occur during diagenesis and dolomitization. To calibrate this effect we induced magnetosome chain collapse in Magnetospirillum magnetotacticum strain MS-1 by progressive sonification and treatment with detergents and monitored the changes with rock magnetic analysis and TEM. Although it has been speculated that the cell wall and associated membrane structures act to prevent magnetosome chain collapse, our data indicate that magnetosome linearity persists long after cells are disrupted. This is consistent with prior observations that in some magnetotcocci the magnetosome chains pass through the cell interior, precluding continuous contact with the cell wall and implying additional support structures exist in some species. Using TEM tomographic reconstructions prepared with a magnetic technique that prevents chain collapse, we examined the three dimensional ultrastructure of magnetosomes without the problem of post-mortem magnetosome motion. This method revealed the presence of an intracellular organic sheath beyond that of actin-like filaments reported recently that follows the chain of magnetosomes, which we postulate evolved to hold the crystals in place and enhances their ability to preserve NRM in sediments. As the genomes of two magnetotactic bacteria contain several apparent homologues of known eukaryotic cytoskeletal proteins, natural selection for magnetotaxis may have played a role in the evolution of precursors to the eukaryotic cytoskeleton. The presence of this sheath is also consistent with the observation of electron translucent material associated with putative magnetofossil chains in ALH84001.

International audience; There are longstanding and ongoing controversies about the abiotic or biological origin of nanocrystals of magnetite. On Earth, magne-totactic bacteria perform biomineralization of intracellular magne-tite nanoparticles under a controlled pathway. These bacteria are ubiquitous in modern natural environments. However, their identification in ancient geological material remains challenging. Together with physical and mineralogical properties, the chemical composition of magnetite was proposed as a promising tracer for bacterial magnetofossil identification, but this had never been explored quantitatively and systematically for many trace elements. Here, we determine the incorporation of 34 trace elements in magnetite in both cases of abiotic aqueous precipitation and of production by the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1. We show that, in biomagnetite, most elements are at least 100 times less concentrated than in abiotic magnetite and we provide a quantitative pattern of this depletion. Furthermore, we propose a previously unidentified method based on strontium and calcium incorporation to identify magnetite produced by magnetotactic bacteria in the geological record. magnetotactic bacteria | magnetite | biomineralization | trace element incorporation

Understanding the magnetic properties of magnetite crystals (Fe3O4) produced by magnetotactic bacteria (MTBs) is of fundamental interest in fields of geosciences, biomineralization, fine particle magnetism, and planetary sciences. The database of bulk magnetic measurements on MTBs is, however, still too sparse to allow for generalizations due to difficulties in obtaining bacteria cells in sufficient quantities from natural environments, and the fact that only a few cultivable strains are available. Here we report the first series of magnetic measurements on two air-dried samples containing solely MTBs (wild-type cocci and Magnetobacterium bavaricum), which were directly isolated from carbonaceous lake sediments. Systematic rock magnetic studies show that: 1) the magnetosomes in cells are dominated by single-domain (SD) magnetite; 2) the samples have delta ratios δFC / δZFC higher than 2; 3) the measured low-temperature remanence cycling curves as well as the first-order-reversal-curve (FORC) diagrams are significantly different to those measured on synthetic SD-magnetite samples; and 4) the Verwey transition temperature (Tv, ∼100 K) of MTB cells is distinctly lower than that from stoichiometric magnetite (Tv, 120–125 K). Our results provide new insights on the magnetic properties of bacterial magnetite and advance the use of magnetic proxies for decoding the paleomagnetic signals of sediments containing bacterial magnetite.

Magnetite is both a common inorganic rock-forming mineral and a biogenic product formed by a diversity of organisms. Magnetotactic bacteria produce intracellular magnetites of high purity and crystallinity (magnetosomes) arranged in linear chains of crystals. Magnetosomes and their fossils (magnetofossils) have been identified using transmission electron microscopy (TEM) in sediments dating back to ∼510–570 Ma, and possibly in 4 Ga carbonates in Martian meteorite ALH84001. We present the results from two rock magnetic analyses—the low-temperature Moskowitz test and ferromagnetic resonance (FMR)—applied to dozens of samples of magnetite and other materials. The magnetites in these samples are of diverse composition, size, shape, and origin: biologically induced (extracellular), biologically controlled (magnetosomes and chiton teeth), magnetofossil, synthetic, and natural inorganic. We confirm that the Moskowitz test is a distinctive indicator for magnetotactic bacteria and provide the first direct experimental evidence that this is accomplished via sensitivity to the magnetosome chain structure. We also demonstrate that the FMR spectra of four different strains of magnetotactic bacteria and a magnetofossil-bearing carbonate have a form distinct from all other samples measured in this study. We suggest that this signature also results from the magnetosomes' unique arrangement in chains. Because FMR can rapidly identify samples with large fractions of intact, isolated magnetosome chains, it could be a powerful tool for identifying magnetofossils in sediments.

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.

We measured pulsed-magnetic-field remanences of individual cells of two types of magnetotactic bacteria. Wild-type magnetic vibrios displayed square remanence curves with the reversal field, Hrev reaching values up to 825 Oe (65.7 kA/m). We attribute the generally high values of Hrev to the elongated shape of the magnetosomes (length-to-width ratio, e≈1.2) and to the comparatively short distances between the magnetosomes (8 nm). Cells of the rod-shaped Magnetobacterium bavaricum, on the other hand, which frequently contain more than 600 magnetosomes per cell, could gradually be demagnetised; the coercivity of remanence, Hcr of individual cells always ranged between 600 and 700 Oe (47.7–55.7 kA/m). The non-square remanence curves of M. bavaricum reflect a distribution of elongations and interactions between adjacent strands of magnetosomes within the braid-like chains.

Although recent studies have revealed more widespread occurrences of magnetofossils in pre-Quaternary sediments than have been previously reported, their significance for paleomagnetic and paleoenvironmental studies is not fully understood. We present a paleo- and rock-magnetic study of late Miocene marine sediments recovered from the Guadalquivir Basin (SW Spain). Well-defined paleomagnetic directions provide a robust magnetostratigraphic chronology for the two studied sediment cores. Rock magnetic results indicate the dominance of intact magnetosome chains throughout the studied sediments. These results provide a link between the highest-quality paleomagnetic directions and higher magnetofossil abundances. We interpret that bacterial magnetite formed in the surface sediment mixed layer and that these magnetic particles gave rise to a paleomagnetic signal in the same way as detrital grains. They, therefore, carry a magnetization that is essentially identical to a post-depositional remanent magnetization, which we term a bio-depositional remanent magnetization. Some studied polarity reversals record paleomagnetic directions with an apparent 60-70 kyr recording delay. Magnetofossils in these cases are interpreted to carry a biogeochemical remanent magnetization that is locked in at greater depth in the sediment column. A sharp decrease in magnetofossil abundance toward the middle of the studied boreholes coincides broadly with a major rise in sediment accumulation rates near the onset of the Messinian salinity crisis (MSC), an event caused by interruption of the connection between the Mediterranean Sea and the Atlantic Ocean. This correlation appears to have resulted from dilution of magnetofossils by enhanced terrigenous inputs that were driven, in turn, by sedimentary changes triggered in the basin at the onset of the MSC. Our results highlight the importance of magnetofossils as carriers of high-quality paleomagnetic and paleoenvironmental signals even in dominantly terrigenous sediments., This study was funded by the Guadaltyc project(MINECO,CGL2012–30875), ARC grant DP120103952,and NSFC grant 41374073.

Of the two nanocrystal (magnetosome) compositions biosynthesized by magnetotactic bacteria (MTB), the magnetic properties of magnetite magnetosomes have been extensively studied using widely available cultures, while those of greigite magnetosomes remain poorly known. Here we have collected uncultivated magnetite- and greigite-producing MTB to determine their magnetic coercivity distribution and ferromagnetic resonance (FMR) spectra and to assess the MTB-associated iron flux. We find that compared with magnetite-producing MTB cultures, FMR spectra of uncultivated MTB are characterized by a wider empirical parameter range, thus complicating the use of FMR for fossilized magnetosome (magnetofossil) detection. Furthermore, in stark contrast to putative Neogene greigite magnetofossil records, the coercivity distributions for greigite-producing MTB are fundamentally left-skewed with a lower median. Lastly, a comparison between the MTB-associated iron flux in the investigated estuary and the pyritic-Fe flux in the Black Sea suggests MTB play an important, but heretofore overlooked role in euxinic marine system iron cycle.

We studied intracellular magnetite particles produced by several morphological types of magnetotactic bacteria including the spirillar (helical) freshwater species, Magnetospirillum magnetotacticum, and four incompletely characterized marine strains: MV-1, a curved rod-shaped bacterium; MC-1 and MC-2, two coccoid (spherical) microorganisms; and MV-4, a spirillum. Particle morphologies, size distributions, and structural features were examined using conventional and high-resolution transmission electron microscopy. The various strains produce crystals with characteristic shapes. All habits can be derived from various combinations of the isometric {111}, {110}, and {100} forms. We compared the size and shape distributions of crystals from magnetotactic bacteria with those of synthetic magnetite grains of similar size and found the biogenic and synthetic distributions to be statistically distinguishable. In particular, the size distributions of the bacterial magnetite crystals are narrower and have a distribution asymmetry that is the opposite of the nonbiogenic sample. The only deviation from ideal structure in the bacterial magnetite seems to be the occurrence of spinel-law twins. Sparse multiple twins were also observed. Because the synthetic magnetite crystals contain twins similar to those in bacteria, in the absence of characteristic chains of crystals, only the size and shape distributions seem to be useful for distinguishing bacterial from nonbiogenic magnetite.

Using transmission electron microscopy, we studied the structures and compositions of Fe sulfides within cells of magnetotactic bacteria that were collected from natural habitats. Ferrimagnetic greigite (Fe3S4) occurred in all types of sulfide-producing magnetotactic bacteria examined. Mackinawite (tetragonal FeS) and, tentatively, sphalerite-type cubic FeS were also identified. In contrast to earlier reports, we did not find pyrite (FeS 2) or pyrrhotite (Fe12xS). Mackinawite converted to greigite over time within the bacteria that were deposited on electron microscope grids and stored in air. Orientation relationships between the two minerals indicate that the cubic-close-packed S substructure remains unchanged during the transformation; only the Fe atoms rearrange. Neither mackinawite nor cubic FeS are magnetic, and yet they are aligned in chains such that when converted to magnetic greigite, the probable easy axis of magnetization, [100], is parallel to the chain direction. The resulting chains of greigite are ultimately responsible for the magnetic dipole moment of the cell. Both greigite and mackinawite magnetosomes can contain Cu, depending on the sampling locality. Because bacterial mackinawite and cubic FeS are unstable over time, only greigite crystals are potentially useful as geological biomarkers.

[1] Single-domain magnetite particles produced by magnetotactic bacteria (MTB) and aligned in chains, called magnetosomes, are potentially important recorders of paleomagnetic, paleoenvironmental and paleolife signals. Rock magnetic properties related to the anisotropy of magnetosome chains have been widely used to identify fossilized magnetosomes (magnetofossils) preserved in geological materials. However, ambiguities exist when linking magnetic properties to the chain structure because of the complexity of chain integrity and magnetostatic interactions among magnetofossils that results from chain collapse during post-depositional diagenesis. In this paper, magnetic properties of three sets of samples containing extracted magnetosomes of the culturedMagnetospirillum magneticumstrain AMB-1 were analyzed to determine how chain integrity and particle concentration influence magnetic properties. Intact MTB and well-dispersed magnetosome chains are characterized by strong magnetic anisotropy and weak magnetostatic interactions, but progressive chain breakup and particle clumping significantly increase the degree of magnetostatic interaction. This results in a change of the magnetic signature toward properties typical of interacting, single-domain particles, i.e., a decrease of the ratio of anhysteretic remanent magnetization to the saturation isothermal remanent magnetization, decreasing in the crossing point of the Wohlfarth-Cisowski test and in the delta ratio between losses of field and zero-field cooled remanent magnetization across the Verwey transition, as well as vertical broadening of the first-order reversal curve distribution. We propose a new diagram that summarizes the Verwey transition properties, with diagnostic limits for intact and collapsed chains of magnetosomes. This diagram can be used, in conjunction with other parameters, to identify unoxidized magnetofossils in sediments and rocks.

We describe pulsed-magnetic-field remanence measurements of individual, killed, undisrupted cells of three different types of magnetotactic bacteria. The measurement technique involved the observation of aligned, individual magnetotactic bacteria with a light microscope as they were subjected to magnetic pulses of increasing amplitude. We show that for MM cells, the hysteresis loop is square, with the coercive field variable from cell to cell. This is consistent with just two magnetization states for the single chain of magnetite particles. For MR and MMP cells, the hysteresis loops are not square, indicating that there are several different magnetization states, and that individual cells can be demagnetized. The coercive fields in the MR and MMP cells are less variable than for the MM cells.

Magnetotactic bacteria biomineralize magnetic minerals with precisely controlled size, morphology, and stoichiometry. These cosmopolitan bacteria are widely observed in aquatic environments. If preserved after burial, the inorganic remains of magnetotactic bacteria act as magnetofossils that record ancient geomagnetic field variations. They also have potential to provide paleoenvironmental information. In contrast to conventional magnetofossils, giant magnetofossils (most likely produced by eukaryotic organisms) have only been reported once before from Paleocene-Eocene Thermal Maximum (PETM; 55.8 Ma) sediments on the New Jersey coastal plain. Here, using transmission electron microscopic observations, we present evidence for abundant giant magnetofossils, including previously reported elongated prisms and spindles, and new giant bullet-shaped magnetite crystals, in the Southern Ocean near Antarctica, not only during the PETM, but also shortly before and after the PETM. Moreover, we have discovered giant bullet-shaped magnetite crystals from the equatorial Indian Ocean during the Mid-Eocene Climatic Optimum (∼40 Ma). Our results indicate a more widespread geographic, environmental, and temporal distribution of giant magnetofossils in the geological record with a link to “hyperthermal” events. Enhanced global weathering during hyperthermals, and expanded suboxic diagenetic environments, probably provided more bioavailable iron that enabled biomineralization of giant magnetofossils. Our micromagnetic modelling indicates the presence of magnetic multi-domain (i.e., not ideal for navigation) and single domain (i.e., ideal for navigation) structures in the giant magnetite particles depending on their size, morphology and spatial arrangement. Different giant magnetite crystal morphologies appear to have had different biological functions, including magnetotaxis and other non-navigational purposes. Our observations suggest that hyperthermals provided ideal conditions for giant magnetofossils, and that these organisms were globally distributed. Much more work is needed to understand the interplay between magnetofossil morphology, climate, nutrient availability, and environmental variability, School of Ocean and Earth Science, National Oceanography Centre, University of Southampton, Reino Unido, Research School of Earth Sciences, The Australian National University, Australia, Grant Institute of Earth Science, University of Edinburgh, Reino Unido, Unidad de Zaragoza, Instituto Geológico y Minero de España, España, Instituto Oceanográfico da Universidade de São Paulo, Brasil, Department of Earth Science and Engineering, Imperial College London, Reino Unido

[1] Magnetic hysteresis measurements of sediments have resulted in widespread reporting of “pseudo-single-domain”-like magnetic properties. In contrast, the ideal single domain (SD) properties that would be expected to be responsible for high quality paleomagnetic records are rare. Determining whether SD particles are rare or common in sediments requires application of techniques that enable discrimination among different magnetic components in a sediment. We apply a range of such techniques and find that SD particles are much more common than has been reported in the literature and that magnetite magnetofossils (the inorganic remains of magnetotactic bacteria) are widely preserved at depth in a range of sediment types, including biogenic pelagic carbonates, lacustrine and marine clays, and possibly even in glaci-marine sediments. Thus, instead of being rarely preserved in the geological record, we find that magnetofossils are widespread. This observation has important implications for our understanding of how sediments become magnetized and highlights the need to develop a more robust basis for understanding how biogenic magnetite contributes to the magnetization of sediments. Magnetofossils also have grain sizes that are substantially smaller than the 1–15μm size range for which there is reasonable empirical support for relative paleointensity studies. The different magnetic response of coexisting fine biogenic and coarser lithogenic particles is likely to complicate relative paleointensity studies. This issue needs much closer attention. Despite the fact that sediments have been subjected to paleomagnetic investigation for over 60 years, much remains to be understood about how they become magnetized.

Since they were first descrbed in 1975 [1], magnetotactic bacteria have been observed in a wide variety of environments, including soils [2], rivers, freshwater lakes and coastal marine sediments [3,4], and in one case at a water depth of about 600 m in a hemipelagic sediment [5]. Here we report the first systematic findings of magnetotactic bacteria in pelagic and hemipelagic sediments of the eastern South Atlantic. Different morphologies were identified (cocci, spirilla, vibrionic and rod-shaped forms) at water depths to about 3000 m on the African continental margin between the equator and 30°S, and on the Walvis Ridge in a pelagic environment about 1400 km off the coast. No actively swimming magnetotactic bacteria could be detected in deeper waters. Magnetotactic bacteria were observed only in the upper 10 cm of the sediments, with the highest concentrations always found in a well-defined narrow subsurface layer. The depth of this layer is dependent on the input and turnover rates of organic matter in the sediment. Measurements of oxygen and nitrate concentrations [6,7] provide an assignment of depth distributions of magnetotactic bacteria to the stratification of terminal electron acceptors in the sediment. The data show clearly that the majority of marine magnetotactic bacteria live in the anaerobic zone, in contrast to former assumptions that they may inhabit microaerobic layers [8–11].

Magnetite (Fe$\_{3}$O$\_{4}$) crystals produced by two strains of cultured vibrioid magnetotactic bacteria were studied by high-resolution transmission electron microscopy (HRTEM). Both magnetotactic strains were characterized by single chains of magnetite crystals aligned along the long axes of the cells. The strains, designated as MV-2 and MV-4, produced crystals that differed markedly in size and morphology. Crystals present in MV-4 cells were generally larger than those in MV-2 cells and displayed significantly smaller aspect ratios. Crystallographic analysis of the magnetosomes of MV-2 revealed an elongated hexagonal habit based on a prism of {110} faces capped by {111} faces. The axis of elongation was parallel to the direction. This morphology closely resembles the crystal shape of magnetosomes in a previously described vibrioid species MV-1. In contrast, magnetosomes of MV-4 possessed a cubo-octahedral morphology which was modified by a small elongation along the direction. Although this morphology has not previously been observed in magnetotactic bacteria, it appears to be intermediate between the regular cubo-octahedral shape of magnetosomes in the cultured species Aquaspirillum magnetotacticum and the extensively elongated cubo-octahedral crystals of a previously studied uncultured ovoid-shaped magnetotactic bacterium. The results support the proposal that the crystal morphologies of bacterial magnetite are strain specific.

We report the discovery of exceptionally large biogenic magnetite crystals in clay-rich sediments spanning the Paleocene–Eocene Thermal Maximum (PETM) in a borehole at Ancora, NJ. Aside from previously described abundant bacterial magnetofossils, electron microscopy reveals novel spearhead-like and spindle-like magnetite up to 4 μm long and hexaoctahedral prisms up to 1.4 μm long. Similar to magnetite produced by magnetotactic bacteria, these single-crystal particles exhibit chemical composition, lattice perfection, and oxygen isotopes consistent with an aquatic origin. Electron holography indicates single-domain magnetization despite their large crystal size. We suggest that the development of a thick suboxic zone with high iron bioavailability—a product of dramatic changes in weathering and sedimentation patterns driven by severe global warming—drove diversification of magnetite-forming organisms, likely including eukaryotes.

[1] The Paleocene-Eocene Thermal Maximum, which occurred � 55.5 Ma, was caused by a massive release of carbon, as indicated by an � 3% negative carbon isotope excursion recorded in the marine, atmospheric, and terrestrial reservoirs. One suggested source for the carbon, a cometary impactor, is based on the sudden appearance and high concentration of single-domain (SD) magnetite in Paleocene-Eocene (P-E) boundary cores from the North Atlantic continental margin. We evaluate the potential sources of SD magnetite at the P-E boundary by presenting new magnetic hysteresis, low-temperature magnetic remanence, and transmission electron microscopy data from the North Atlantic coastal ocean. Our results show a similar increase in SD material but demonstrate that the magnetic material has a biogenic origin. These findings indicate that the high concentrations of SD magnetite immediately above the P-E boundary are the result of unusual accumulations and/or preservation of magnetotactic bacteria. Such bacteria typically occupy the oxic-anoxic transition zone near the sediment-water interface or in the water column. The high abundances of SD magnetite in sediments from across the shelf may be an artifact of nonsteady state redox conditions and exceptional preservation of SD magnetite. It may also indicate that the oxic-anoxic redox boundary shifted into the water column. The latter explanation implies transient eutrophy of the coastal ocean in this region, most likely due to seasonally enhanced runoff, and increased stratification and nutrient loading.

Previous workers identified a magnetically anomalous clay layer deposited on the northern United States Atlantic Coastal Plain during the Paleocene-Eocene Thermal Maximum (PETM). The finding inspired the highly controversial hypothesis that a cometary impact triggered the PETM. Here we present ferromagnetic resonance (FMR), isothermal and anhysteretic remanent magnetization, first order reversal curve, and transmission electron microscopy analyses of late Paleocene and early Eocene sediments in drillcore from Ancora, New Jersey. A novel paleogeographic analysis applying a recent paleomagnetic pole from the Faeroe Islands indicates that New Jersey during the initial Eocene had a ~6-9 degrees lower paleolatitude (~27.3 degrees for Ancora) and a more zonal shoreline trace than in conventional reconstructions. Our investigations of the PETM clay from Ancora reveal abundant magnetite nanoparticles bearing signature traits of crystals produced by magnetotactic bacteria. This result, the first identification of ancient biogenic magnetite using FMR, argues that the anomalous magnetic properties of the PETM sediments are not produced by an impact. They instead reflect environmental changes along the eastern margin of North America during the PETM that led to enhanced production and/or preservation of magnetofossils.

[1] First-order reversal curve (FORC) diagrams are rapidly becoming a standard tool for characterizing magnetic particles because they simultaneously incorporate information regarding magnetostatic interaction and domain states. The simplest interpretation of FORC diagrams of single-domain (SD) particles is based on the Neel interpretation of Preisach theory, which predicts that the FORC function is the product of a coercivity and an interaction field distribution. Although the underlying assumptions of this interpretation are not correct, a strictly quantitative model of weakly interacting SD grains proves that the distributions of coercivities and interaction fields can be retrieved from a FORC diagram. To test this model, we present the possibility of a quantitative interpretation of FORC diagrams, and we present measurements of samples containing magnetosomes from cultures of magnetotactic bacteria and from a lake sediment. Two samples are investigated under the electron microscope to characterize the geometrical arrangement of the particles. We find that the clustering of otherwise similar particles has a strong influence on FORC diagrams. We also obtained a crude estimate of packing densities form the FORC diagrams, which were consistent with transmission electron microscopy observations and measurements of the anhysteretic remanent magnetization.