Renaissance for magnetotactic bacteria in astrobiology.

Capable of forming magnetofossils similar to some magnetite nanocrystals observed in the Martian meteorite ALH84001, magnetotactic bacteria (MTB) once occupied a special position in the field of astrobiology during the 1990s and 2000s. This flourish of interest in putative Martian magnetofossils faded from all but the experts studying magnetosome formation, based on claims that abiotic processes could produce magnetosome-like magnetite crystals. Recently, the rapid growth in our knowledge of the extreme environments in which MTB thrive and their phylogenic heritage, leads us to advocate for a renaissance of MTB in astrobiology. In recent decades, magnetotactic members have been discovered alive in natural extreme environments with wide ranges of salinity (up to 90 g L-1), pH (1-10), and temperature (0-70 °C). Additionally, some MTB populations are found to be able to survive irradiated, desiccated, metal-rich, hypomagnetic, or microgravity conditions, and are capable of utilizing simple inorganic compounds such as sulfate and nitrate. Moreover, MTB likely emerged quite early in Earth's history, coinciding with a period when the Martian surface was covered with liquid water as well as a strong magnetic field. MTB are commonly discovered in suboxic or oxic-anoxic interfaces in aquatic environments or sediments similar to ancient crater lakes on Mars, such as Gale crater and Jezero crater. Taken together, MTB can be exemplary model microorganisms in astrobiology research, and putative ancient Martian life, if it ever occurred, could plausibly have included magnetotactic microorganisms. Furthermore, we summarize multiple typical biosignatures that can be applied for the detection of ancient MTB on Earth and extraterrestrial MTB-like life. We suggest transporting MTB to space stations and simulation chambers to further investigate their tolerance potential and distinctive biosignatures to aid in understanding the evolutionary history of MTB and the potential of magnetofossils as an extraterrestrial biomarker.

Response to comment on "Reexamination of 2.5-Ga 'whiff' of oxygen interval points to anoxic ocean before GOE".

Sedimentological, textural, and microscale analyses of the Mount McRae Shale revealed a complex postdepositional history, previously unrecognized in bulk geochemical studies. We found that metal enrichments in the shale do not reside with depositional organic carbon, as previously proposed by Anbar et al., but with late-stage pyrite, compromising claims for a "whiff" of oxygen ~50 million years before the Great Oxygenation Event.

Reexamination of 2.5-Ga "whiff" of oxygen interval points to anoxic ocean before GOE.

Transient appearances of oxygen have been inferred before the Great Oxygenation Event (GOE) [∼2.3 billion years (Ga) ago] based on redox-sensitive elements such as Mo and S­most prominently from the ∼2.5-Ga Mount McRae Shale in Western Australia. We present new spatially resolved data including synchrotron-based x-ray spectroscopy and secondary ion mass spectrometry to characterize the petrogenesis of the Mount McRae Shale. Sediments were primarily composed of organic matter and volcanic ash (a potential source of Mo), with U-Pb ages revealing extremely low sedimentation rates. Catagenesis created bedding-parallel microfractures, which subsequently acted as fluid pathways for metasomatic alteration and recent oxidative weathering. Our collective observations suggest that the bulk chemical datasets pointing toward a "whiff" of oxygen developed during postdepositional events. Nonzero Δ33S in trace-metal­poor, early diagenetic pyrite and the unusually enriched organic carbon at low sedimentation rates instead suggest that environmental oxygen levels were negligible ∼150 million years before the GOE.

A Late Cretaceous true polar wander oscillation.

True polar wander (TPW), or planetary reorientation, is well documented for other planets and moons and for Earth at present day with satellites, but testing its prevalence in Earth's past is complicated by simultaneous motions due to plate tectonics. Debate has surrounded the existence of Late Cretaceous TPW ca. 84 million years ago (Ma). Classic palaeomagnetic data from the Scaglia Rossa limestone of Italy are the primary argument against the existence of ca. 84 Ma TPW. Here we present a new high-resolution palaeomagnetic record from two overlapping stratigraphic sections in Italy that provides evidence for a ~12° TPW oscillation from 86 to 78 Ma. This observation represents the most recent large-scale TPW documented and challenges the notion that the spin axis has been largely stable over the past 100 million years.

On the origin of microbial magnetoreception.

A broad range of organisms, from prokaryotes to higher animals, have the ability to sense and utilize Earth's geomagnetic field-a behavior known as magnetoreception. Although our knowledge of the physiological mechanisms of magnetoreception has increased substantially over recent decades, the origin of this behavior remains a fundamental question in evolutionary biology. Despite this, there is growing evidence that magnetic iron mineral biosynthesis by prokaryotes may represent the earliest form of biogenic magnetic sensors on Earth. Here, we integrate new data from microbiology, geology and nanotechnology, and propose that initial biomineralization of intracellular iron nanoparticles in early life evolved as a mechanism for mitigating the toxicity of reactive oxygen species (ROS), as ultraviolet radiation and free-iron-generated ROS would have been a major environmental challenge for life on early Earth. This iron-based system could have later been co-opted as a magnetic sensor for magnetoreception in microorganisms, suggesting an origin of microbial magnetoreception as the result of the evolutionary process of exaptation.

Transduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain.

Magnetoreception, the perception of the geomagnetic field, is a sensory modality well-established across all major groups of vertebrates and some invertebrates, but its presence in humans has been tested rarely, yielding inconclusive results. We report here a strong, specific human brain response to ecologically-relevant rotations of Earth-strength magnetic fields. Following geomagnetic stimulation, a drop in amplitude of electroencephalography (EEG) alpha-oscillations (8-13 Hz) occurred in a repeatable manner. Termed alpha-event-related desynchronization (alpha-ERD), such a response has been associated previously with sensory and cognitive processing of external stimuli including vision, auditory and somatosensory cues. Alpha-ERD in response to the geomagnetic field was triggered only by horizontal rotations when the static vertical magnetic field was directed downwards, as it is in the Northern Hemisphere; no brain responses were elicited by the same horizontal rotations when the static vertical component was directed upwards. This implicates a biological response tuned to the ecology of the local human population, rather than a generic physical effect. Biophysical tests showed that the neural response was sensitive to static components of the magnetic field. This rules out all forms of electrical induction (including artifacts from the electrodes) which are determined solely on dynamic components of the field. The neural response was also sensitive to the polarity of the magnetic field. This rules out free-radical "quantum compass" mechanisms like the cryptochrome hypothesis, which can detect only axial alignment. Ferromagnetism remains a viable biophysical mechanism for sensory transduction and provides a basis to start the behavioral exploration of human magnetoreception.

Magnetic control of heterogeneous ice nucleation with nanophase magnetite: Biophysical and agricultural implications.

In supercooled water, ice nucleation is a stochastic process that requires ∼250-300 molecules to transiently achieve structural ordering before an embryonic seed crystal can nucleate. This happens most easily on crystalline surfaces, in a process termed heterogeneous nucleation; without such surfaces, water droplets will supercool to below -30 °C before eventually freezing homogeneously. A variety of fundamental processes depends on heterogeneous ice nucleation, ranging from desert-blown dust inducing precipitation in clouds to frost resistance in plants. Recent experiments have shown that crystals of nanophase magnetite (Fe3O4) are powerful nucleation sites for this heterogeneous crystallization of ice, comparable to other materials like silver iodide and some cryobacterial peptides. In natural materials containing magnetite, its ferromagnetism offers the possibility that magneto-mechanical motion induced by external oscillating magnetic fields could act to disrupt the water-crystal interface, inhibiting the heterogeneous nucleation process in subfreezing water and promoting supercooling. For this to act, the magneto-mechanical rotation of the particles should be higher than the magnitude of Brownian motions. We report here that 10-Hz precessing magnetic fields, at strengths of 1 mT and above, on ∼50-nm magnetite crystals dispersed in ultrapure water, meet these criteria and do indeed produce highly significant supercooling. Using these rotating magnetic fields, we were able to elicit supercooling in two representative plant and animal tissues (celery and bovine muscle), both of which have detectable, natural levels of ferromagnetic material. Tailoring magnetic oscillations for the magnetite particle size distribution in different tissues could maximize this supercooling effect.

Origin of microbial biomineralization and magnetotaxis during the Archean.

Microbes that synthesize minerals, a process known as microbial biomineralization, contributed substantially to the evolution of current planetary environments through numerous important geochemical processes. Despite its geological significance, the origin and evolution of microbial biomineralization remain poorly understood. Through combined metagenomic and phylogenetic analyses of deep-branching magnetotactic bacteria from the Nitrospirae phylum, and using a Bayesian molecular clock-dating method, we show here that the gene cluster responsible for biomineralization of magnetosomes, and the arrangement of magnetosome chain(s) within cells, both originated before or near the Archean divergence between the Nitrospirae and Proteobacteria This phylogenetic divergence occurred well before the Great Oxygenation Event. Magnetotaxis likely evolved due to environmental pressures conferring an evolutionary advantage to navigation via the geomagnetic field. Earth's dynamo must therefore have been sufficiently strong to sustain microbial magnetotaxis in the Archean, suggesting that magnetotaxis coevolved with the geodynamo over geological time.

A first test of the hypothesis of biogenic magnetite-based heterogeneous ice-crystal nucleation in cryopreservation.

An outstanding biophysical puzzle is focused on the apparent ability of weak, extremely low-frequency oscillating magnetic fields to enhance cryopreservation of many biological tissues. A recent theory holds that these weak magnetic fields could be inhibiting ice-crystal nucleation on the nanocrystals of biological magnetite (Fe3O4, an inverse cubic spinel) that are present in many plant and animal tissues by causing them to oscillate. In this theory, magnetically-induced mechanical oscillations disrupt the ability of water molecules to nucleate on the surface of the magnetite nanocrystals. However, the ability of the magnetite crystal lattice to serve as a template for heterogeneous ice crystal nucleation is as yet unknown, particularly for particles in the 10-100 nm size range. Here we report that the addition of trace-amounts of finely-dispersed magnetite into ultrapure water samples reduces strongly the incidence of supercooling, as measured in experiments conducted using a controlled freezing apparatus with multiple thermocouples. SQUID magnetometry was used to quantify nanogram levels of magnetite in the water samples. We also report a relationship between the volume change of ice, and the degree of supercooling, that may indicate lower degassing during the crystallization of supercooled water. In addition to supporting the role of ice-crystal nucleation by biogenic magnetite in many tissues, magnetite nanocrystals could provide inexpensive, non-toxic, and non-pathogenic ice nucleating agents needed in a variety of industrial processes, as well as influencing the dynamics of ice crystal nucleation in many natural environments.

Timescales of Oxygenation Following the Evolution of Oxygenic Photosynthesis.

Among the most important bioenergetic innovations in the history of life was the invention of oxygenic photosynthesis-autotrophic growth by splitting water with sunlight-by Cyanobacteria. It is widely accepted that the invention of oxygenic photosynthesis ultimately resulted in the rise of oxygen by ca. 2.35 Gya, but it is debated whether this occurred more or less immediately as a proximal result of the evolution of oxygenic Cyanobacteria or whether they originated several hundred million to more than one billion years earlier in Earth history. The latter hypothesis involves a prolonged period during which oxygen production rates were insufficient to oxidize the atmosphere, potentially due to redox buffering by reduced species such as higher concentrations of ferrous iron in seawater. To examine the characteristic timescales for environmental oxygenation following the evolution of oxygenic photosynthesis, we applied a simple mathematical approach that captures many of the salient features of the major biogeochemical fluxes and reservoirs present in Archean and early Paleoproterozoic surface environments. Calculations illustrate that oxygenation would have overwhelmed redox buffers within ~100 kyr following the emergence of oxygenic photosynthesis, a geologically short amount of time unless rates of primary production were far lower than commonly expected. Fundamentally, this result arises because of the multiscale nature of the carbon and oxygen cycles: rates of gross primary production are orders of magnitude too fast for oxygen to be masked by Earth's geological buffers, and can only be effectively matched by respiration at non-negligible O2 concentrations. These results suggest that oxygenic photosynthesis arose shortly before the rise of oxygen, not hundreds of millions of years before it.

SQUID-SIMS is a useful approach to uncover primary signals in the Archean sulfur cycle.

Many aspects of Earth's early sulfur cycle, from the origin of mass-anomalous fractionations to the degree of biological participation, remain poorly understood--in part due to complications from postdepositional diagenetic and metamorphic processes. Using a combination of scanning high-resolution magnetic superconducting quantum interference device (SQUID) microscopy and secondary ion mass spectrometry (SIMS) of sulfur isotopes ((32)S, (33)S, and (34)S), we examined drill core samples from slope and basinal environments adjacent to a major Late Archean (∼2.6-2.5 Ga) marine carbonate platform from South Africa. Coupled with petrography, these techniques can untangle the complex history of mineralization in samples containing diverse sulfur-bearing phases. We focused on pyrite nodules, precipitated in shallow sediments. These textures record systematic spatial differences in both mass-dependent and mass-anomalous sulfur-isotopic composition over length scales of even a few hundred microns. Petrography and magnetic imaging demonstrate that mass-anomalous fractionations were acquired before burial and compaction, but also show evidence of postdepositional alteration 500 million y after deposition. Using magnetic imaging to screen for primary phases, we observed large spatial gradients in Δ(33)S (>4‰) in nodules, pointing to substantial environmental heterogeneity and dynamic mixing of sulfur pools on geologically rapid timescales. In other nodules, large systematic radial δ(34)S gradients (>20‰) were observed, from low values near their centers increasing to high values near their rims. These fractionations support hypotheses that microbial sulfate reduction was an important metabolism in organic-rich Archean environments--even in an Archean ocean basin dominated by iron chemistry.

A ferromagnetic model for the action of electric and magnetic fields in cryopreservation.

Recent discussions in the literature have questioned the ability of electromagnetic exposure to inhibit ice crystal formation in supercooled water. Here we note that strong electric fields are able to disrupt the surface boundary layer of inert air on the surface of materials, promoting higher rates of heat transport. We also note that most biological tissues contain ferromagnetic materials, both biologically precipitated magnetite (Fe3O4) as well as environmental contaminants that get accidentally incorporated into living systems. Although present at trace levels, the number density of these particulates is high, and they have extraordinarily strong interactions with weak, low-frequency magnetic fields of the sort involved in claims of electromagnetic cryopreservation. Magnetically-induced mechanical oscillation of these particles provides a plausible mechanism for the disruption of ice-crystal nucleation in supercooled water.

Manganese-oxidizing photosynthesis before the rise of cyanobacteria.

The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O2--multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redox-sensitive detrital grains--reveal that the original Mn-oxide phases were not produced by reactions with O2, which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.

Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells.

Over the past 50 y, behavioral experiments have produced a large body of evidence for the existence of a magnetic sense in a wide range of animals. However, the underlying sensory physiology remains poorly understood due to the elusiveness of the magnetosensory structures. Here we present an effective method for isolating and characterizing potential magnetite-based magnetoreceptor cells. In essence, a rotating magnetic field is employed to visually identify, within a dissociated tissue preparation, cells that contain magnetic material by their rotational behavior. As a tissue of choice, we selected trout olfactory epithelium that has been previously suggested to host candidate magnetoreceptor cells. We were able to reproducibly detect magnetic cells and to determine their magnetic dipole moment. The obtained values (4 to 100 fAm(2)) greatly exceed previous estimates (0.5 fAm(2)). The magnetism of the cells is due to a µm-sized intracellular structure of iron-rich crystals, most likely single-domain magnetite. In confocal reflectance imaging, these produce bright reflective spots close to the cell membrane. The magnetic inclusions are found to be firmly coupled to the cell membrane, enabling a direct transduction of mechanical stress produced by magnetic torque acting on the cellular dipole in situ. Our results show that the magnetically identified cells clearly meet the physical requirements for a magnetoreceptor capable of rapidly detecting small changes in the external magnetic field. This would also explain interference of ac powerline magnetic fields with magnetoreception, as reported in cattle.

Searching for biosignatures using electron paramagnetic resonance (EPR) analysis of manganese oxides.

Manganese oxide (Mn oxide) minerals from bacterial sources produce electron paramagnetic resonance (EPR) spectral signatures that are mostly distinct from those of synthetic simulants and abiogenic mineral Mn oxides. Biogenic Mn oxides exhibit only narrow EPR spectral linewidths (∼500 G), whereas abiogenic Mn oxides produce spectral linewidths that are 2-6 times broader and range from 1200 to 3000 G. This distinction is consistent with X-ray structural observations that biogenic Mn oxides have abundant layer site vacancies and edge terminations and are mostly of single ionic species [i.e., Mn(IV)], all of which favor narrow EPR linewidths. In contrast, abiogenic Mn oxides have fewer lattice vacancies, larger particle sizes, and mixed ionic species [Mn(III) and Mn(IV)], which lead to the broader linewidths. These properties could be utilized in the search for extraterrestrial physicochemical biosignatures, for example, on Mars missions that include a miniature version of an EPR spectrometer.

A quantitative assessment of torque-transducer models for magnetoreception.

Although ferrimagnetic material appears suitable as a basis of magnetic field perception in animals, it is not known by which mechanism magnetic particles may transduce the magnetic field into a nerve signal. Provided that magnetic particles have remanence or anisotropic magnetic susceptibility, an external magnetic field will exert a torque and may physically twist them. Several models of such biological magnetic-torque transducers on the basis of magnetite have been proposed in the literature. We analyse from first principles the conditions under which they are viable. Models based on biogenic single-domain magnetite prove both effective and efficient, irrespective of whether the magnetic structure is coupled to mechanosensitive ion channels or to an indirect transduction pathway that exploits the strayfield produced by the magnetic structure at different field orientations. On the other hand, torque-detector models that are based on magnetic multi-domain particles in the vestibular organs turn out to be ineffective. Also, we provide a generic classification scheme of torque transducers in terms of axial or polar output, within which we discuss the results from behavioural experiments conducted under altered field conditions or with pulsed fields. We find that the common assertion that a magnetoreceptor based on single-domain magnetite could not form the basis for an inclination compass does not always hold.