A 200-million-year delay in permanent atmospheric oxygenation.

The rise of atmospheric oxygen fundamentally changed the chemistry of surficial environments and the nature of Earth's habitability1. Early atmospheric oxygenation occurred over a protracted period of extreme climatic instability marked by multiple global glaciations2,3, with the initial rise of oxygen concentration to above 10-5 of the present atmospheric level constrained to about 2.43 billion years ago4,5. Subsequent fluctuations in atmospheric oxygen levels have, however, been reported to have occurred until about 2.32 billion years ago4, which represents the estimated timing of irreversible oxygenation of the atmosphere6,7. Here we report a high-resolution reconstruction of atmospheric and local oceanic redox conditions across the final two glaciations of the early Palaeoproterozoic era, as documented by marine sediments from the Transvaal Supergroup, South Africa. Using multiple sulfur isotope and iron-sulfur-carbon systematics, we demonstrate continued oscillations in atmospheric oxygen levels after about 2.32 billion years ago that are linked to major perturbations in ocean redox chemistry and climate. Oxygen levels thus fluctuated across the threshold of 10-5 of the present atmospheric level for about 200 million years, with permanent atmospheric oxygenation finally arriving with the Lomagundi carbon isotope excursion at about 2.22 billion years ago, some 100 million years later than currently estimated.

A case for an active eukaryotic marine biosphere during the Proterozoic era.

The microfossil record demonstrates the presence of eukaryotic organisms in the marine ecosystem by about 1,700 million years ago (Ma). Despite this, steranes, a biomarker indicator of eukaryotic organisms, do not appear in the rock record until about 780 Ma in what is known as the "rise of algae." Before this, it is argued that eukaryotes were minor ecosystem members, with prokaryotes dominating both primary production and ecosystem dynamics. In this view, the rise of algae was possibly sparked by increased nutrient availability supplying the higher nutrient requirements of eukaryotic algae. Here, we challenge this view. We use a size-based ecosystem model to show that the size distribution of preserved eukaryotic microfossils from 1,700 Ma and onward required an active eukaryote ecosystem complete with phototrophy, osmotrophy, phagotrophy, and mixotrophy. Model results suggest that eukaryotes accounted for one-half or more of the living biomass, with eukaryotic algae contributing to about one-half of total marine primary production. These ecosystems lived with deep-water phosphate levels of at least 10% of modern levels. The general lack of steranes in the pre-780-Ma rock record could be a result of poor preservation.

Microbe Profile: Nitrosopumilus maritimus.

Nitrosopumilus maritimus is a marine ammonia-oxidizing archaeon with a high affinity for ammonia. It fixes carbon via a modified hydroxypropionate/hydroxybutyrate cycle and shows weak utilization of cyanate as a supplementary energy and nitrogen source. When oxygen is depleted, N. maritimus produces its own oxygen, which may explain its regular occurrence in anoxic waters. Several enzymes of the ammonia oxidation and oxygen production pathways remain to be identified.

Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago.

Evidence for macroscopic life in the Paleoproterozoic Era comes from 1.8 billion-year-old (Ga) compression fossils [Han TM, Runnegar B (1992) Science 257:232-235; Knoll et al. (2006) Philos Trans R Soc Lond B 361:1023-1038], Stirling biota [Bengtson S et al. (2007) Paleobiology 33:351-381], and large colonial organisms exhibiting signs of coordinated growth from the 2.1-Ga Francevillian series, Gabon. Here we report on pyritized string-shaped structures from the Francevillian Basin. Combined microscopic, microtomographic, geochemical, and sedimentologic analyses provide evidence for biogenicity, and syngenicity and suggest that the structures underwent fossilization during early diagenesis close to the sediment-water interface. The string-shaped structures are up to 6 mm across and extend up to 170 mm through the strata. Morphological and 3D tomographic reconstructions suggest that the producer may have been a multicellular or syncytial organism able to migrate laterally and vertically to reach food resources. A possible modern analog is the aggregation of amoeboid cells into a migratory slug phase in cellular slime molds at times of starvation. This unique ecologic window established in an oxygenated, shallow-marine environment represents an exceptional record of the biosphere following the crucial changes that occurred in the atmosphere and ocean in the aftermath of the great oxidation event (GOE).

A Mesoproterozoic iron formation.

We describe a 1,400 million-year old (Ma) iron formation (IF) from the Xiamaling Formation of the North China Craton. We estimate this IF to have contained at least 520 gigatons of authigenic Fe, comparable in size to many IFs of the Paleoproterozoic Era (2,500-1,600 Ma). Therefore, substantial IFs formed in the time window between 1,800 and 800 Ma, where they are generally believed to have been absent. The Xiamaling IF is of exceptionally low thermal maturity, allowing the preservation of organic biomarkers and an unprecedented view of iron-cycle dynamics during IF emplacement. We identify tetramethyl aryl isoprenoid (TMAI) biomarkers linked to anoxygenic photosynthetic bacteria and thus phototrophic Fe oxidation. Although we cannot rule out other pathways of Fe oxidation, iron and organic matter likely deposited to the sediment in a ratio similar to that expected for anoxygenic photosynthesis. Fe reduction was likely a dominant and efficient pathway of organic matter mineralization, as indicated by organic matter maturation by Rock Eval pyrolysis combined with carbon isotope analyses: Indeed, Fe reduction was seemingly as efficient as oxic respiration. Overall, this Mesoproterozoic-aged IF shows many similarities to Archean-aged (>2,500 Ma) banded IFs (BIFs), but with an exceptional state of preservation, allowing an unprecedented exploration of Fe-cycle dynamics in IF deposition.

Atmospheric oxygenation three billion years ago.

It is widely assumed that atmospheric oxygen concentrations remained persistently low (less than 10(-5) times present levels) for about the first 2 billion years of Earth's history. The first long-term oxygenation of the atmosphere is thought to have taken place around 2.3 billion years ago, during the Great Oxidation Event. Geochemical indications of transient atmospheric oxygenation, however, date back to 2.6-2.7 billion years ago. Here we examine the distribution of chromium isotopes and redox-sensitive metals in the approximately 3-billion-year-old Nsuze palaeosol and in the near-contemporaneous Ijzermyn iron formation from the Pongola Supergroup, South Africa. We find extensive mobilization of redox-sensitive elements through oxidative weathering. Furthermore, using our data we compute a best minimum estimate for atmospheric oxygen concentrations at that time of 3 × 10(-4) times present levels. Overall, our findings suggest that there were appreciable levels of atmospheric oxygen about 3 billion years ago, more than 600 million years before the Great Oxidation Event and some 300-400 million years earlier than previous indications for Earth surface oxygenation.

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters.

A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O2) sensitivity of these processes down to the O2 concentrations present in the OMZ core (<10 nmol⋅L(-1)) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O2 levels between 5 nmol⋅L(-1) and 20 µmol⋅L(-1) Rates of both processes were detectable in the low nanomolar range (5-33 nmol⋅L(-1) O2), but demonstrated a strong dependence on O2 concentrations with apparent half-saturation constants (Kms) of 333 ± 130 nmol⋅L(-1) O2 for ammonium oxidation and 778 ± 168 nmol⋅L(-1) O2 for nitrite oxidation assuming one-component Michaelis-Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis-Menten model, indicating a high-affinity component with a Km of just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O2 affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O2 is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.

Sufficient oxygen for animal respiration 1,400 million years ago.

The Mesoproterozoic Eon [1,600-1,000 million years ago (Ma)] is emerging as a key interval in Earth history, with a unique geochemical history that might have influenced the course of biological evolution on Earth. Indeed, although this time interval is rather poorly understood, recent chromium isotope results suggest that atmospheric oxygen levels were <0.1% of present levels, sufficiently low to have inhibited the evolution of animal life. In contrast, using a different approach, we explore the distribution and enrichments of redox-sensitive trace metals in the 1,400 Ma sediments of Unit 3 of the Xiamaling Formation, North China Block. Patterns of trace metal enrichments reveal oxygenated bottom waters during deposition of the sediments, and biomarker results demonstrate the presence of green sulfur bacteria in the water column. Thus, we document an ancient oxygen minimum zone. We develop a simple, yet comprehensive, model of marine carbon-oxygen cycle dynamics to show that our geochemical results are consistent with atmospheric oxygen levels >4% of present-day levels. Therefore, in contrast to previous suggestions, we show that there was sufficient oxygen to fuel animal respiration long before the evolution of animals themselves.

Orbital forcing of climate 1.4 billion years ago.

Fluctuating climate is a hallmark of Earth. As one transcends deep into Earth time, however, both the evidence for and the causes of climate change become difficult to establish. We report geochemical and sedimentological evidence for repeated, short-term climate fluctuations from the exceptionally well-preserved ∼1.4-billion-year-old Xiamaling Formation of the North China Craton. We observe two patterns of climate fluctuations: On long time scales, over what amounts to tens of millions of years, sediments of the Xiamaling Formation record changes in geochemistry consistent with long-term changes in the location of the Xiamaling relative to the position of the Intertropical Convergence Zone. On shorter time scales, and within a precisely calibrated stratigraphic framework, cyclicity in sediment geochemical dynamics is consistent with orbital control. In particular, sediment geochemical fluctuations reflect what appear to be orbitally forced changes in wind patterns and ocean circulation as they influenced rates of organic carbon flux, trace metal accumulation, and the source of detrital particles to the sediment.

Oxygen requirements of the earliest animals.

A rise in the oxygen content of the atmosphere and oceans is one of the most popular explanations for the relatively late and abrupt appearance of animal life on Earth. In this scenario, Earth's surface environment failed to meet the high oxygen requirements of animals up until the middle to late Neoproterozoic Era (850-542 million years ago), when oxygen concentrations sufficiently rose to permit the existence of animal life for the first time. Although multiple lines of geochemical evidence support an oxygenation of the Ediacaran oceans (635-542 million years ago), roughly corresponding with the first appearance of metazoans in the fossil record, the oxygen requirements of basal animals remain unclear. Here we show that modern demosponges, serving as analogs for early animals, can survive under low-oxygen conditions of 0.5-4.0% present atmospheric levels. Because the last common ancestor of metazoans likely exhibited a physiology and morphology similar to that of a modern sponge, its oxygen demands may have been met well before the enhanced oxygenation of the Ediacaran Period. Therefore, the origin of animals may not have been triggered by a contemporaneous rise in the oxygen content of the atmosphere and oceans. Instead, other ecological and developmental processes are needed to adequately explain the origin and earliest evolution of animal life on Earth.

Metabolomics Reveals Cryptic Interactive Effects of Species Interactions and Environmental Stress on Nitrogen and Sulfur Metabolism in Seagrass.

Eutrophication of estuaries and coastal seas is accelerating, increasing light stress on subtidal marine plants and changing their interactions with other species. To date, we have limited understanding of how such variations in environmental and biological stress modify the impact of interactions among foundational species and eventually affect ecosystem health. Here, we used metabolomics to assess the impact of light reductions on interactions between the seagrass Zostera marina, an important habitat-forming marine plant, and the abundant and commercially important blue mussel Mytilus edulis. Plant performance varied with light availability but was unaffected by the presence of mussels. Metabolomic analysis, on the other hand, revealed an interaction between light availability and presence of M. edulis on seagrass metabolism. Under high light, mussels stimulated seagrass nitrogen and energy metabolism. Conversely, in low light mussels impeded nitrogen and energy metabolism, and enhanced responses against sulfide toxicity, causing inhibited oxidative energy metabolism and tissue degradation. Metabolomic analysis thereby revealed cryptic changes to seagrass condition that could not be detected by traditional approaches. Our findings suggest that coastal eutrophication and associated reductions in light may shift seagrass-bivalve interactions from mutualistic to antagonistic, which is important for conservation management of seagrass meadows.

Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago.

The evidence for macroscopic life during the Palaeoproterozoic era (2.5-1.6 Gyr ago) is controversial. Except for the nearly 2-Gyr-old coil-shaped fossil Grypania spiralis, which may have been eukaryotic, evidence for morphological and taxonomic biodiversification of macroorganisms only occurs towards the beginning of the Mesoproterozoic era (1.6-1.0 Gyr). Here we report the discovery of centimetre-sized structures from the 2.1-Gyr-old black shales of the Palaeoproterozoic Francevillian B Formation in Gabon, which we interpret as highly organized and spatially discrete populations of colonial organisms. The structures are up to 12 cm in size and have characteristic shapes, with a simple but distinct ground pattern of flexible sheets and, usually, a permeating radial fabric. Geochemical analyses suggest that the sediments were deposited under an oxygenated water column. Carbon and sulphur isotopic data indicate that the structures were distinct biogenic objects, fossilized by pyritization early in the formation of the rock. The growth patterns deduced from the fossil morphologies suggest that the organisms showed cell-to-cell signalling and coordinated responses, as is commonly associated with multicellular organization. The Gabon fossils, occurring after the 2.45-2.32-Gyr increase in atmospheric oxygen concentration, may be seen as ancient representatives of multicellular life, which expanded so rapidly 1.5 Gyr later, in the Cambrian explosion.

Oxygen and animal evolution: did a rise of atmospheric oxygen "trigger" the origin of animals?

Recent studies challenge the classical view that the origin of animal life was primarily controlled by atmospheric oxygen levels. For example, some modern sponges, representing early-branching animals, can live under 200 times less oxygen than currently present in the atmosphere - levels commonly thought to have been maintained prior to their origination. Furthermore, it is increasingly argued that the earliest animals, which likely lived in low oxygen environments, played an active role in constructing the well-oxygenated conditions typical of the modern oceans. Therefore, while oxygen is still relevant to understanding early animal evolution, the relationships between the two might be less straightforward than previously thought.

Sulfur isotopes in coal constrain the evolution of the Phanerozoic sulfur cycle.

Sulfate is the second most abundant anion (behind chloride) in modern seawater, and its cycling is intimately coupled to the cycling of organic matter and oxygen at the Earth's surface. For example, the reduction of sulfide by microbes oxidizes vast amounts of organic carbon and the subsequent reaction of sulfide with iron produces pyrite whose burial in sediments is an important oxygen source to the atmosphere. The concentrations of seawater sulfate and the operation of sulfur cycle have experienced dynamic changes through Earth's history, and our understanding of this history is based mainly on interpretations of the isotope record of seawater sulfates and sedimentary pyrites. The isotope record, however, does not give a complete picture of the ancient sulfur cycle. This is because, in standard isotope mass balance models, there are more variables than constraints. Typically, in interpretations of the isotope record and in the absence of better information, one assumes that the isotopic composition of the input sulfate to the oceans has remained constant through time. It is argued here that this assumption has a constraint over the last 390 Ma from the isotopic composition of sulfur in coal. Indeed, these compositions do not deviate substantially from the modern surface-water input to the oceans. When applied to mass balance models, these results support previous interpretations of sulfur cycle operation and counter recent suggestions that sulfate has been a minor player in sulfur cycling through the Phanerozoic Eon.

Oxygen dynamics in the aftermath of the Great Oxidation of Earth's atmosphere.

The oxygen content of Earth's atmosphere has varied greatly through time, progressing from exceptionally low levels before about 2.3 billion years ago, to much higher levels afterward. In the absence of better information, we usually view the progress in Earth's oxygenation as a series of steps followed by periods of relative stasis. In contrast to this view, and as reported here, a dynamic evolution of Earth's oxygenation is recorded in ancient sediments from the Republic of Gabon from between about 2,150 and 2,080 million years ago. The oldest sediments in this sequence were deposited in well-oxygenated deep waters whereas the youngest were deposited in euxinic waters, which were globally extensive. These fluctuations in oxygenation were likely driven by the comings and goings of the Lomagundi carbon isotope excursion, the longest-lived positive δ(13)C excursion in Earth history, generating a huge oxygen source to the atmosphere. As the Lomagundi event waned, the oxygen source became a net oxygen sink as Lomagundi organic matter became oxidized, driving oxygen to low levels; this state may have persisted for 200 million years.

Microbial oceanography of anoxic oxygen minimum zones.

Vast expanses of oxygen-deficient and nitrite-rich water define the major oxygen minimum zones (OMZs) of the global ocean. They support diverse microbial communities that influence the nitrogen economy of the oceans, contributing to major losses of fixed nitrogen as dinitrogen (N(2)) and nitrous oxide (N(2)O) gases. Anaerobic microbial processes, including the two pathways of N(2) production, denitrification and anaerobic ammonium oxidation, are oxygen-sensitive, with some occurring only under strictly anoxic conditions. The detection limit of the usual method (Winkler titrations) for measuring dissolved oxygen in seawater, however, is much too high to distinguish low oxygen conditions from true anoxia. However, new analytical technologies are revealing vanishingly low oxygen concentrations in nitrite-rich OMZs, indicating that these OMZs are essentially anoxic marine zones (AMZs). Autonomous monitoring platforms also reveal previously unrecognized episodic intrusions of oxygen into the AMZ core, which could periodically support aerobic metabolisms in a typically anoxic environment. Although nitrogen cycling is considered to dominate the microbial ecology and biogeochemistry of AMZs, recent environmental genomics and geochemical studies show the presence of other relevant processes, particularly those associated with the sulfur and carbon cycles. AMZs correspond to an intermediate state between two "end points" represented by fully oxic systems and fully sulfidic systems. Modern and ancient AMZs and sulfidic basins are chemically and functionally related. Global change is affecting the magnitude of biogeochemical fluxes and ocean chemical inventories, leading to shifts in AMZ chemistry and biology that are likely to continue well into the future.

Mechanism for Burgess Shale-type preservation.

Exceptionally preserved fossil biotas of the Burgess Shale and a handful of other similar Cambrian deposits provide rare but critical insights into the early diversification of animals. The extraordinary preservation of labile tissues in these geographically widespread but temporally restricted soft-bodied fossil assemblages has remained enigmatic since Walcott's initial discovery in 1909. Here, we demonstrate the mechanism of Burgess Shale-type preservation using sedimentologic and geochemical data from the Chengjiang, Burgess Shale, and five other principal Burgess Shale-type deposits. Sulfur isotope evidence from sedimentary pyrites reveals that the exquisite fossilization of organic remains as carbonaceous compressions resulted from early inhibition of microbial activity in the sediments by means of oxidant deprivation. Low sulfate concentrations in the global ocean and low-oxygen bottom water conditions at the sites of deposition resulted in reduced oxidant availability. Subsequently, rapid entombment of fossils in fine-grained sediments and early sealing of sediments by pervasive carbonate cements at bed tops restricted oxidant flux into the sediments. A permeability barrier, provided by bed-capping cements that were emplaced at the seafloor, is a feature that is shared among Burgess Shale-type deposits, and resulted from the unusually high alkalinity of Cambrian oceans. Thus, Burgess Shale-type preservation of soft-bodied fossil assemblages worldwide was promoted by unique aspects of early Paleozoic seawater chemistry that strongly impacted sediment diagenesis, providing a fundamentally unique record of the immediate aftermath of the "Cambrian explosion."

Towards a quantitative understanding of the late Neoproterozoic carbon cycle.

The cycles of carbon and oxygen at the Earth surface are intimately linked, where the burial of organic carbon into sediments represents a source of oxygen to the surface environment. This coupling is typically quantified through the isotope records of organic and inorganic carbon. Yet, the late Neoproterozoic Eon, the time when animals first evolved, experienced wild isotope fluctuations which do not conform to our normal understanding of the carbon cycle and carbon-oxygen coupling. We interpret these fluctuations with a new carbon cycle model and demonstrate that all of the main features of the carbonate and organic carbon isotope record can be explained by the release of methane hydrates from an anoxic dissolved organic carbon-rich ocean into an atmosphere containing oxygen levels considerably less than today.

Strong linkage between benthic oxygen uptake and bacterial tetraether lipids in deep-sea trench regions.

Oxygen in marine sediments regulates many key biogeochemical processes, playing a crucial role in shaping Earth's climate and benthic ecosystems. In this context, branched glycerol dialkyl glycerol tetraethers (brGDGTs), essential biomarkers in paleoenvironmental research, exhibit an as-yet-unresolved association with sediment oxygen conditions. Here, we investigated brGDGTs in sediments from three deep-sea regions (4045 to 10,100 m water depth) dominated by three respective trench systems and integrated the results with in situ oxygen microprofile data. Our results demonstrate robust correlations between diffusive oxygen uptake (DOU) obtained from microprofiles and brGDGT methylation and isomerization degrees, indicating their primary production within sediments and their strong linkage with microbial diagenetic activity. We establish a quantitative relationship between the Isomerization and Methylation index of Branched Tetraethers (IMBT) and DOU, suggesting its potential validity across deep-sea environments. Increased brGDGT methylation and isomerization likely enhance the fitness of source organisms in deep-sea habitats. Our study positions brGDGTs as a promising tool for quantifying benthic DOU in deep-sea settings, where DOU is a key metric for assessing sedimentary organic carbon degradation and microbial activity.