Identification and characterization of magnetotactic Gammaproteobacteria from a salt evaporation pool, Bohai Bay, China.

Magnetotactic bacteria (MTB) are phylogenetically diverse prokaryotes that can produce intracellular chain-assembled nanocrystals of magnetite (Fe3 O4 ) or greigite (Fe3 S4 ). Compared with their wide distribution in the Alpha-, Eta- and Delta-proteobacteria classes, few MTB strains have been identified in the Gammaproteobacteria class, resulting in limited knowledge of bacterial diversity and magnetosome biomineralization within this phylogenetic branch. Here, we identify two magnetotactic Gammaproteobacteria strains (tentatively named FZSR-1 and FZSR-2 respectively) from a salt evaporation pool in Bohai Bay, at the Fuzhou saltern, Dalian City, eastern China. Phylogenetic analysis indicates that strain FZSR-2 is the same species as strains SHHR-1 and SS-5, which were discovered previously from brackish and hypersaline environments respectively. Strain FZSR-1 represents a novel species. Compared with strains FZSR-2, SHHR-1 and SS-5 in which magnetite particles are assembled into a single chain, FZSR-1 cells form relatively narrower magnetite nanoparticles that are often organized into double chains. We find a good relationship between magnetite morphology within strains FZSR-2, SHHR-1 and SS-5 and the salinity of the environment in which they live. This study expands the bacterial diversity of magnetotactic Gammaproteobacteria and provides new insights into magnetosome biomineralization within magnetotactic Gammaproteobacteria.

Identification of sulfate-reducing magnetotactic bacteria via a group-specific 16S rDNA primer and correlative fluorescence and electron microscopy: Strategy for culture-independent study.

Magnetotactic bacteria (MTB) biomineralize intracellular magnetic nanocrystals and swim along geomagnetic field lines. While few axenic MTB cultures exist, living cells can be separated magnetically from natural environments for analysis. The bacterial universal 27F/1492R primer pair has been used widely to amplify nearly full-length 16S rRNA genes and to provide phylogenetic portraits of MTB communities. However, incomplete coverage and amplification biases inevitably prevent detection of some phylogenetically specific or non-abundant MTB. Here, we propose a new formulation of the upstream 390F primer that we combined with the downstream 1492R primer to specifically amplify 1100-bp 16S rRNA gene sequences of sulfate-reducing MTB in freshwater sediments from Lake Weiyanghu, Xi'an, northwestern China. With correlative fluorescence in situ hybridization and scanning/transmission electron microscopy, three novel MTB strains (WYHR-2, WYHR-3 and WYHR-4) from the Desulfobacterota phylum were identified phylogenetically and structurally at the single-cell level. Strain WYHR-2 produces bullet-shaped magnetosome magnetite, while the other two strains produce both cubic/prismatic greigite and bullet-shaped magnetite. Our results expand knowledge of bacterial diversity and magnetosome biomineralization of sulfate-reducing MTB. We also propose a general strategy for identifying and characterizing uncultured MTB from natural environments.

Diverse phylogeny and morphology of magnetite biomineralized by magnetotactic cocci.

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.

A Novel Magnetotactic Alphaproteobacterium Producing Intracellular Magnetite and Calcium-Bearing Minerals.

Magnetotactic bacteria (MTB) are prokaryotes that form intracellular magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals with tailored sizes, often in chain configurations. Such magnetic particles are each surrounded by a lipid bilayer membrane, called a magnetosome, and provide a model system for studying the formation and function of specialized internal structures in prokaryotes. Using fluorescence-coupled scanning electron microscopy, we identified a novel magnetotactic spirillum, XQGS-1, from freshwater Xingqinggong Lake, Xi'an City, Shaanxi Province, China. Phylogenetic analyses based on 16S rRNA gene sequences indicate that strain XQGS-1 represents a novel genus of the Alphaproteobacteria class in the Proteobacteria phylum. Transmission electron microscopy analyses reveal that strain XQGS-1 forms on average 17 ± 3 magnetite magnetosome particles with an ideal truncated octahedral morphology, with an average length and width of 88.3 ± 11.7 nm and 83.3 ± 11.0 nm, respectively. They are tightly organized into a single chain along the cell long axis close to the concave side of the cell. Intrachain magnetic interactions likely result in these large equidimensional magnetite crystals behaving as magnetically stable single-domain particles that enable bacterial magnetotaxis. Combined structural and chemical analyses demonstrate that XQGS-1 cells also biomineralize intracellular amorphous calcium phosphate (2 to 3 granules per cell; 90.5- ± 19.3-nm average size) and weakly crystalline calcium carbonate (2 to 3 granules per cell; 100.4- ± 21.4-nm average size) in addition to magnetite. Our results expand the taxonomic diversity of MTB and provide evidence for intracellular calcium phosphate biomineralization in MTB. IMPORTANCE Biomineralization is a widespread process in eukaryotes that form shells, teeth, or bones. It also occurs commonly in prokaryotes, resulting in more than 60 known minerals formed by different bacteria under wide-ranging conditions. Among them, magnetotactic bacteria (MTB) are remarkable because they might represent the earliest organisms that biomineralize intracellular magnetic iron minerals (i.e., magnetite [Fe3O4] or greigite [Fe3S4]). Here, we report a novel magnetotactic spirillum (XQGS-1) that is phylogenetically affiliated with the Alphaproteobacteria class. In addition to magnetite crystals, XQGS-1 cells form intracellular submicrometer calcium carbonate and calcium phosphate granules. This finding supports the view that MTB are also an important microbial group for intracellular calcium carbonate and calcium phosphate biomineralization.

Multidecadally resolved polarity oscillations during a geomagnetic excursion.

Polarity reversals of the geomagnetic field have occurred through billions of years of Earth history and were first revealed in the early 20th century. Almost a century later, details of transitional field behavior during geomagnetic reversals and excursions remain poorly known. Here, we present a multidecadally resolved geomagnetic excursion record from a radioisotopically dated Chinese stalagmite at 107-91 thousand years before present with age precision of several decades. The duration of geomagnetic directional oscillations ranged from several centuries at 106-103 thousand years before present to millennia at 98-92 thousand years before present, with one abrupt reversal transition occurring in one to two centuries when the field was weakest. These features indicate prolonged geodynamo instability. Repeated asymmetrical interhemispheric polarity drifts associated with weak dipole fields likely originated in Earth's deep interior. If such rapid polarity changes occurred in future, they could severely affect satellites and human society.

Magnetic Vortex States in Toroidal Iron Oxide Nanoparticles: Combining Micromagnetics with Tomography.

Iron oxide nanorings have great promise for biomedical applications because of their magnetic vortex state, which endows them with a low remanent magnetization while retaining a large saturation magnetization. Here we use micromagnetic simulations to predict the exact shapes that can sustain magnetic vortices, using a toroidal model geometry with variable diameter, ring thickness, and ring eccentricity. Our model phase diagram is then compared with simulations of experimental geometries obtained by electron tomography. High axial eccentricity and low ring thickness are found to be key factors for forming vortex states and avoiding net-magnetized metastable states. We also find that while defects from a perfect toroidal geometry increase the stray field associated with the vortex state, they can also make the vortex state more energetically accessible. These results constitute an important step toward optimizing the magnetic behavior of toroidal iron oxide nanoparticles.

Phylogenetic and Structural Identification of a Novel Magnetotactic Deltaproteobacteria Strain, WYHR-1, from a Freshwater Lake.

Magnetotactic bacteria (MTB) are phylogenetically diverse prokaryotes that are able to biomineralize intracellular, magnetic chains of magnetite or greigite nanocrystals called magnetosomes. Simultaneous characterization of MTB phylogeny and biomineralization is crucial but challenging because most MTB are extremely difficult to culture. We identify a large rod, bean-like MTB (tentatively named WYHR-1) from freshwater sediments of Weiyang Lake, Xi'an, China, using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Phylogenetic analysis of 16S rRNA gene sequences indicates that WYHR-1 is a novel genus from the Deltaproteobacteria class. Transmission electron microscope observations reveal that WYHR-1 cells contain tens of magnetite magnetosomes that are organized into a single chain bundle along the cell long axis. Mature WYHR-1 magnetosomes are bullet-shaped, straight, and elongated along the [001] direction, with a large flat end terminated by a {100} face at the base and a conical top. This crystal morphology is distinctively different from bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum. This indicates that WYHR-1 may have a different crystal growth process and mechanism from other species, which results from species-specific magnetosome biomineralization in MTB.IMPORTANCE Magnetotactic bacteria (MTB) represent a model system for understanding biomineralization and are also studied intensively in biogeomagnetic and paleomagnetic research. However, many uncultured MTB strains have not been identified phylogenetically or investigated structurally at the single-cell level, which limits comprehensive understanding of MTB diversity and their role in biomineralization. We have identified a novel MTB strain, WYHR-1, from a freshwater lake using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Our analyses further indicate that strain WYHR-1 represents a novel genus from the Deltaproteobacteria class. In contrast to bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum, WYHR-1 magnetosomes are bullet-shaped, straight, and highly elongated along the [001] direction, are terminated by a large {100} face at their base, and have a conical top. Our findings imply that, consistent with phylogenetic diversity of MTB, bullet-shaped magnetosomes have diverse crystal habits and growth patterns.

An updated age for the Xujiayao hominin from the Nihewan Basin, North China: Implications for Middle Pleistocene human evolution in East Asia.

The Xujiayao site in the Nihewan Basin (North China) is one of the most important Paleolithic sites in East Asia. Twenty Homo fossils, which were previously assigned to an archaic Homo sapiens group, have been excavated along with more than 30,000 lithic artifacts and ∼5000 mammalian fossil specimens. Dating of the Xujiayao hominin has been pursued since its excavation in the 1970s, but its age has remained controversial because of limitations of the dating techniques that have been applied to available materials. Here, we report new ages for the Xujiayao hominin based on combined electron spin resonance (ESR) dating of quartz in the sediments and high-resolution magnetostratigraphy of the fluvio-lacustrine sequence. The magnetostratigraphy suggests that the upper Matuyama and Brunhes polarity chrons are recorded at Xujiayao. The ESR dating results indicate a pooled average age of 260-370 ka for the Homo-bearing layer, which is consistent with its position within the middle Brunhes normal polarity chron indicated by magnetostratigraphy. This age estimate makes the Xujiayao hominin among the oldest mid-Pleistocene hominins with derived Neanderthal traits in East Asia. This age is consistent with the time when early Denisovans, a sister group of Neanderthals, appeared and colonized eastern Eurasia. Our updated age and the Neanderthal-like traits of the Xujiayao Homo fossils, particularly the Denisovan-like molar teeth, make it possible that the Xujiayao hominin could represent an early Denisovan.

Origin of Magnetism in Hydrothermally Aged 2-Line Ferrihydrite Suspensions.

As an iron oxyhydroxide, nanosized ferrihydrite (Fh) is important in Earth science, biology, and industrial applications. However, its basic structure and origin of its magnetism have long been debated. We integrate synchrotron-based techniques to explore the chemical structures of 2-line ferrihydrite and to determine the origin of its magnetism during hydrothermal aging in air. Our results demonstrate that both the magnetism and X-ray magnetic circular dichroism (XMCD) signal of 2-line ferrihydrite are enhanced with aging time, and that XMCD spectral patterns resemble that of maghemite (γ-Fe2O3) rather than magnetite (Fe3O4). Fe L-edge and K-edge X-ray absorption spectroscopy (XAS) further indicate formation of both maghemite and hematite (α-Fe2O3) with increasing concentrations with longer hydrothermal aging time. Thus, magnetic enhancement with longer hydrothermal aging time is attributed to increasing maghemite concentration instead of a magnetically ordered ferrihydrite as previously reported. Moreover, L-edge and K-edge XAS spectra with different probing depths yield different ratios of these Fe oxides, which suggest the formation of a core (ferrihydrite-rich)-shell (with a mixture of both allotropes; α-Fe2O3 and γ-Fe2O3) structure during hydrothermal aging. Our results provide insights into the chemical evolution of 2-line ferrihydrite that reveal unambiguously the origin of its magnetism.

Volcanic ash layers illuminate the resilience of Neanderthals and early modern humans to natural hazards.

Marked changes in human dispersal and development during the Middle to Upper Paleolithic transition have been attributed to massive volcanic eruption and/or severe climatic deterioration. We test this concept using records of volcanic ash layers of the Campanian Ignimbrite eruption dated to ca. 40,000 y ago (40 ka B.P.). The distribution of the Campanian Ignimbrite has been enhanced by the discovery of cryptotephra deposits (volcanic ash layers that are not visible to the naked eye) in archaeological cave sequences. They enable us to synchronize archaeological and paleoclimatic records through the period of transition from Neanderthal to the earliest anatomically modern human populations in Europe. Our results confirm that the combined effects of a major volcanic eruption and severe climatic cooling failed to have lasting impacts on Neanderthals or early modern humans in Europe. We infer that modern humans proved a greater competitive threat to indigenous populations than natural disasters.

Orbital- and millennial-scale Asian winter monsoon variability across the Pliocene-Pleistocene glacial intensification.

Intensification of northern hemisphere glaciation (iNHG), ~2.7 million years ago (Ma), led to establishment of the Pleistocene to present-day bipolar icehouse state. Here we document evolution of orbital- and millennial-scale Asian winter monsoon (AWM) variability across the iNHG using a palaeomagnetically dated centennial-resolution grain size record between 3.6 and 1.9 Ma from a previously undescribed loess-palaeosol/red clay section on the central Chinese Loess Plateau. We find that the late Pliocene-early Pleistocene AWM was characterized by combined 41-kyr and ~100-kyr cycles, in response to ice volume and atmospheric CO2 forcing. Northern hemisphere ice sheet expansion, which was accompanied by an atmospheric CO2 concentration decline, substantially increased glacial AWM intensity  and its orbitally oscillating amplitudes across the iNHG. Superposed on orbital variability, we find that millennial AWM intensity fluctuations persisted during both the warmer (higher-CO2) late Pliocene and colder (lower-CO2) early Pleistocene, in response to both external astronomical forcing and internal climate dynamics.

East Asian winter monsoon intensification over the Northwest Pacific Ocean driven by late Miocene atmospheric CO2 decline.

East Asian winter monsoon (EAWM) activity has had profound effects on environmental change throughout East Asia and the western Pacific. Much attention has been paid to Quaternary EAWM evolution, while long-term EAWM fluctuation characteristics and drivers remain unclear, particularly during the late Miocene when marked global climate and Asian paleogeographic changes occurred. To clarify understanding of late Miocene EAWM evolution, we developed a high-precision 9-million-year-long stacked EAWM record from Northwest Pacific Ocean abyssal sediments based on environmental magnetism, sedimentology, and geochemistry, which reveals a strengthened late Miocene EAWM. Our paleoclimate simulations also indicate that atmospheric CO2 decline played a vital role in this EAWM intensification over the Northwest Pacific Ocean compared to other factors, including central Asian orogenic belt and northeastern Tibetan Plateau uplift and Antarctic ice-sheet expansion. Our results expand understanding of EAWM evolution from inland areas to the open ocean and indicate the importance of atmospheric CO2 fluctuations on past EAWM variability over large spatial scales.

Continental ice in Greenland during the Eocene and Oligocene.

The Eocene and Oligocene epochs (approximately 55 to 23 million years ago) comprise a critical phase in Earth history. An array of geological records supported by climate modelling indicates a profound shift in global climate during this interval, from a state that was largely free of polar ice caps to one in which ice sheets on Antarctica approached their modern size. However, the early glaciation history of the Northern Hemisphere is a subject of controversy. Here we report stratigraphically extensive ice-rafted debris, including macroscopic dropstones, in late Eocene to early Oligocene sediments from the Norwegian-Greenland Sea that were deposited between about 38 and 30 million years ago. Our data indicate sediment rafting by glacial ice, rather than sea ice, and point to East Greenland as the likely source. Records of this type from one site alone cannot be used to determine the extent of ice involved. However, our data suggest the existence of (at least) isolated glaciers on Greenland about 20 million years earlier than previously documented, at a time when temperatures and atmospheric carbon dioxide concentrations were substantially higher.

Key gene networks that control magnetosome biomineralization in magnetotactic bacteria.

Magnetotactic bacteria (MTB) are a group of phylogenetically and morphologically diverse prokaryotes that have the capability of sensing Earth's magnetic field via nanocrystals of magnetic iron minerals. These crystals are enclosed within intracellular membranes or organelles known as magnetosomes and enable a sensing function known as magnetotaxis. Although MTB were discovered over half a century ago, the study of the magnetosome biogenesis and organization remains limited to a few cultured MTB strains. Here, we present an integrative genomic and phenomic analysis to investigate the genetic basis of magnetosome biomineralization in both cultured and uncultured strains from phylogenetically diverse MTB groups. The magnetosome gene contents/networks of strains are correlated with magnetic particle morphology and chain configuration. We propose a general model for gene networks that control/regulate magnetosome biogenesis and chain assembly in MTB systems.

Phylogenetics and biomineralization of a novel magnetotactic Gammaproteobacterium from a freshwater lake in Beijing, China.

Magnetotactic bacteria (MTB) have the remarkable capability of producing intracellularly membrane-enveloped magnetic nanocrystals (i.e. magnetosomes) and swimming along geomagnetic field lines. Despite more than 50 years of research, bacterial diversity and magnetosome biomineralization within MTB are relatively less known in the Gammaproteobacteria class than other groups. This is incompatible with the status of Gammaproteobacteria as the most diverse class of gram-negative bacteria with a number of ecologically important bacteria. Here, we identify a novel MTB strain YYHR-1 affiliated with the Gammaproteobacteria class of the Pseudomonadota phylum from a freshwater lake. In YYHR-1, most magnetosome crystals are organized into a long chain aligned along the cell long axis; unusually, a few small superparamagnetic crystals are located at the side of the chain, off the main chain axis. Micromagnetic simulations indicate that magnetostatic interactions among adjacent crystals within a chain reduce the Gibbs energy to enhance chain stability. Genomic analysis suggests that duplication of magnetosome gene clusters may result in off-chain magnetosomes formation. By integrating available genomic data from Gammaproteobacteria, the phylogenetic position of MTB in this class is reassigned here. Our new findings expand knowledge about MTB diversity and magnetosome biomineralization, and deepen understanding of the phylogenetics of the Gammaproteobacteria.

Indian Ocean glacial deoxygenation and respired carbon accumulation during mid-late Quaternary ice ages.

Reconstructions of ocean oxygenation are critical for understanding the role of respired carbon storage in regulating atmospheric CO2. Independent sediment redox proxies are essential to assess such reconstructions. Here, we present a long magnetofossil record from the eastern Indian Ocean in which we observe coeval magnetic hardening and enrichment of larger, more elongated, and less oxidized magnetofossils during glacials compared to interglacials over the last ~900 ka. Our multi-proxy records of redox-sensitive magnetofossils, trace element concentrations, and benthic foraminiferal Δδ13C consistently suggest a recurrence of lower O2 in the glacial Indian Ocean over the last 21 marine isotope stages, as has been reported for the Atlantic and Pacific across the last glaciation. Consistent multi-proxy documentation of this repeated oxygen decline strongly supports the hypothesis that increased Indian Ocean glacial carbon storage played a significant role in atmospheric CO2 cycling and climate change over recent glacial/interglacial timescales.

Magnetotactic bacteria and magnetofossils: ecology, evolution and environmental implications.

Magnetotactic bacteria (MTB) are a group of phylogenetically diverse and morphologically varied microorganisms with a magnetoresponsive capability called magnetotaxis or microbial magnetoreception. MTB are a distinctive constituent of the microbiome of aquatic ecosystems because they use Earth's magnetic field to align themselves in a north or south facing direction and efficiently navigate to their favored microenvironments. They have been identified worldwide from diverse aquatic and waterlogged microbiomes, including freshwater, saline, brackish and marine ecosystems, and some extreme environments. MTB play important roles in the biogeochemical cycling of iron, sulphur, phosphorus, carbon and nitrogen in nature and have been recognized from in vitro cultures to sequester heavy metals like selenium, cadmium, and tellurium, which makes them prospective candidate organisms for aquatic pollution bioremediation. The role of MTB in environmental systems is not limited to their lifespan; after death, fossil magnetosomal magnetic nanoparticles (known as magnetofossils) are a promising proxy for recording paleoenvironmental change and geomagnetic field history. Here, we summarize the ecology, evolution, and environmental function of MTB and the paleoenvironmental implications of magnetofossils in light of recent discoveries.

Sea level and deep-sea temperature reconstructions suggest quasi-stable states and critical transitions over the past 40 million years.

Sea level and deep-sea temperature variations are key indicators of global climate changes. For continuous records over millions of years, deep-sea carbonate microfossil-based δ18O (δc) records are indispensable because they reflect changes in both deep-sea temperature and seawater δ18O (δw); the latter are related to ice volume and, thus, to sea level changes. Deep-sea temperature is usually resolved using elemental ratios in the same benthic microfossil shells used for δc, with linear scaling of residual δw to sea level changes. Uncertainties are large and the linear-scaling assumption remains untested. Here, we present a new process-based approach to assess relationships between changes in sea level, mean ice sheet δ18O, and both deep-sea δw and temperature and find distinct nonlinearity between sea level and δw changes. Application to δc records over the past 40 million years suggests that Earth's climate system has complex dynamical behavior, with threshold-like adjustments (critical transitions) that separate quasi-stable deep-sea temperature and ice-volume states.

Global warming-induced Asian hydrological climate transition across the Miocene-Pliocene boundary.

Across the Miocene-Pliocene boundary (MPB; 5.3 million years ago, Ma), late Miocene cooling gave way to the early-to-middle Pliocene Warm Period. This transition, across which atmospheric CO2 concentrations increased to levels similar to present, holds potential for deciphering regional climate responses in Asia-currently home to more than half of the world's population- to global climate change. Here we find that CO2-induced MPB warming both increased summer monsoon moisture transport over East Asia, and enhanced aridification over large parts of Central Asia by increasing evaporation, based on integration of our ~1-2-thousand-year (kyr) resolution summer monsoon records from the Chinese Loess Plateau aeolian red clay with existing terrestrial records, land-sea correlations, and climate model simulations. Our results offer palaeoclimate-based support for 'wet-gets-wetter and dry-gets-drier' projections of future regional hydroclimate responses to sustained anthropogenic forcing. Moreover, our high-resolution monsoon records reveal a dynamic response to eccentricity modulation of solar insolation, with predominant 405-kyr and ~100-kyr periodicities between 8.1 and 3.4 Ma.