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.

Massive perturbations to atmospheric sulfur in the aftermath of the Chicxulub impact.

SignificanceSulfur isotopes confirm a key role for atmospheric sulfur gases in climatic cooling, mass extinction, and the demise of dinosaurs and other global biota after the Chicxulub bolide impact at the Cretaceous-Paleogene boundary. The sulfur isotope anomalies are confined to beds containing ejecta and, in the immediately overlying sediments, are temporally unrelated to known episodes of volcanism that also bracket this event, further addressing the controversial role of the Deccan Traps in the extinction.

Onset of the aerobic nitrogen cycle during the Great Oxidation Event.

The rise of oxygen on the early Earth (about 2.4 billion years ago) caused a reorganization of marine nutrient cycles, including that of nitrogen, which is important for controlling global primary productivity. However, current geochemical records lack the temporal resolution to address the nature and timing of the biogeochemical response to oxygenation directly. Here we couple records of ocean redox chemistry with nitrogen isotope (15N/14N) values from approximately 2.31-billion-year-old shales of the Rooihoogte and Timeball Hill formations in South Africa, deposited during the early stages of the first rise in atmospheric oxygen on the Earth (the Great Oxidation Event). Our data fill a gap of about 400 million years in the temporal 15N/14N record and provide evidence for the emergence of a pervasive aerobic marine nitrogen cycle. The interpretation of our nitrogen isotope data in the context of iron speciation and carbon isotope data suggests biogeochemical cycling across a dynamic redox boundary, with primary productivity fuelled by chemoautotrophic production and a nitrogen cycle dominated by nitrogen loss processes using newly available marine oxidants. This chemostratigraphic trend constrains the onset of widespread nitrate availability associated with ocean oxygenation. The rise of marine nitrate could have allowed for the rapid diversification and proliferation of nitrate-using cyanobacteria and, potentially, eukaryotic phytoplankton.

The Great Oxidation Event preceded a Paleoproterozoic "snowball Earth".

The inability to resolve the exact temporal relationship between two pivotal events in Earth history, the Paleoproterozoic Great Oxidation Event (GOE) and the first "snowball Earth" global glaciation, has precluded assessing causality between changing atmospheric composition and ancient climate change. Here we present temporally resolved quadruple sulfur isotope measurements (δ34S, ∆33S, and ∆36S) from the Paleoproterozoic Seidorechka and Polisarka Sedimentary Formations on the Fennoscandian Shield, northwest Russia, that address this issue. Sulfides in the former preserve evidence of mass-independent fractionation of sulfur isotopes (S-MIF) falling within uncertainty of the Archean reference array with a ∆36S/∆33S slope of -1.8 and have small negative ∆33S values, whereas in the latter mass-dependent fractionation of sulfur isotopes (S-MDF) is evident, with a ∆36S/∆33S slope of -8.8. These trends, combined with geochronological constraints, place the S-MIF/S-MDF transition, the key indicator of the GOE, between 2,501.5 ± 1.7 Ma and 2,434 ± 6.6 Ma. These are the tightest temporal and stratigraphic constraints yet for the S-MIF/S-MDF transition and show that its timing in Fennoscandia is consistent with the S-MIF/S-MDF transition in North America and South Africa. Further, the glacigenic part of the Polisarka Formation occurs 60 m above the sedimentary succession containing S-MDF signals. Hence, our findings confirm unambiguously that the S-MIF/S-MDF transition preceded the Paleoproterozoic snowball Earth. Resolution of this temporal relationship constrains cause-and-effect drivers of Earth's oxygenation, specifically ruling out conceptual models in which global glaciation precedes or causes the evolution of oxygenic photosynthesis.

Spatial Variability of Microbial Communities and Salt Distributions Across a Latitudinal Aridity Gradient in the Atacama Desert.

Over the past 150 million years, the Chilean Atacama Desert has been transformed into one of the most inhospitable landscapes by geophysical changes, which makes it an ideal Mars analog that has been explored for decades. However, a heavy rainfall that occurred in the Atacama in 2017 provides a unique opportunity to study the response of resident extremophiles to rapid environmental change associated with excessive water and salt shock. Here we combine mineral/salt composition measurements, amendment cell culture experiments, and next-generation sequencing analyses to study the variations in salts and microbial communities along a latitudinal aridity gradient of the Atacama Desert. In addition, we examine the reshuffling of Atacama microbiomes after the rainfall event. Analysis of microbial community composition revealed that soils within the southern arid desert were consistently dominated by Actinobacteria, Chloroflexi, Proteobacteria, Firmicutes, Bacteroidetes, Gemmatimonadetes, Planctomycetes, and Acidobacteria, and Verrucomicrobia. Intriguingly, the hyperarid microbial consortia exhibited a similar pattern to the more southern desert. Salts at the shallow subsurface were dissolved and leached down to a deeper layer, challenging indigenous microorganisms with the increasing osmotic stress. Microbial viability was found to change with aridity and rainfall events. This study sheds light on the structure of xerotolerant, halotolerant, and radioresistant microbiomes from the hyperarid northern desert to the less arid southern transition region, as well as their response to changes in water availability.

Biological regulation of atmospheric chemistry en route to planetary oxygenation.

Emerging evidence suggests that atmospheric oxygen may have varied before rising irreversibly ∼2.4 billion years ago, during the Great Oxidation Event (GOE). Significantly, however, pre-GOE atmospheric aberrations toward more reducing conditions-featuring a methane-derived organic-haze-have recently been suggested, yet their occurrence, causes, and significance remain underexplored. To examine the role of haze formation in Earth's history, we targeted an episode of inferred haze development. Our redox-controlled (Fe-speciation) carbon- and sulfur-isotope record reveals sustained systematic stratigraphic covariance, precluding nonatmospheric explanations. Photochemical models corroborate this inference, showing Δ36S/Δ33S ratios are sensitive to the presence of haze. Exploiting existing age constraints, we estimate that organic haze developed rapidly, stabilizing within ∼0.3 ± 0.1 million years (Myr), and persisted for upward of ∼1.4 ± 0.4 Myr. Given these temporal constraints, and the elevated atmospheric CO2 concentrations in the Archean, the sustained methane fluxes necessary for haze formation can only be reconciled with a biological source. Correlative δ13COrg and total organic carbon measurements support the interpretation that atmospheric haze was a transient response of the biosphere to increased nutrient availability, with methane fluxes controlled by the relative availability of organic carbon and sulfate. Elevated atmospheric methane concentrations during haze episodes would have expedited planetary hydrogen loss, with a single episode of haze development providing up to 2.6-18 × 1018 moles of O2 equivalents to the Earth system. Our findings suggest the Neoarchean likely represented a unique state of the Earth system where haze development played a pivotal role in planetary oxidation, hastening the contingent biological innovations that followed.

Biogeodynamics: bridging the gap between surface and deep Earth processes.

Life is sustained by a critical and not insubstantial set of elements, nearly all of which are contained within large rock reservoirs and cycled between Earth's surface and the mantle via subduction zone plate tectonics. Over geologic time scales, plate tectonics plays a critical role in recycling subducted bioactive elements lost to the mantle back to the ocean-biosphere system, via outgassing and volcanism. Biology additionally relies on tectonic processes to supply rock-bound 'nutrients' to marine and terrestrial ecosystems via uplift and erosion. Thus, the development of modern-style plate tectonics and the generation of stable continents were key events in the evolution of the biosphere on Earth, and similar tectonic processes could be crucial for the development of habitability on exoplanets. Despite this vital 'biogeodynamic' connection, directly testing hypotheses about feedbacks between the deep Earth and the biosphere remains challenging. Here, I discuss potential avenues to bridge the biosphere-geosphere gap, focusing specifically on the global cycling and bioavailability of major nutrients (nitrogen and phosphorus) over geologic time scales.This article is part of a discussion meeting issue 'Earth dynamics and the development of plate tectonics'.

Pathways for Neoarchean pyrite formation constrained by mass-independent sulfur isotopes.

It is generally thought that the sulfate reduction metabolism is ancient and would have been established well before the Neoarchean. It is puzzling, therefore, that the sulfur isotope record of the Neoarchean is characterized by a signal of atmospheric mass-independent chemistry rather than a strong overprint by sulfate reducers. Here, we present a study of the four sulfur isotopes obtained using secondary ion MS that seeks to reconcile a number of features seen in the Neoarchean sulfur isotope record. We suggest that Neoarchean ocean basins had two coexisting, significantly sized sulfur pools and that the pathways forming pyrite precursors played an important role in establishing how the isotopic characteristics of each of these pools was transferred to the sedimentary rock record. One of these pools is suggested to be a soluble (sulfate) pool, and the other pool (atmospherically derived elemental sulfur) is suggested to be largely insoluble and unreactive until it reacts with hydrogen sulfide. We suggest that the relative contributions of these pools to the formation of pyrite depend on both the accumulation of the insoluble pool and the rate of sulfide production in the pyrite-forming environments. We also suggest that the existence of a significant nonsulfate pool of reactive sulfur has masked isotopic evidence for the widespread activity of sulfate reducers in the rock record.

Evolution of the crustal phosphorus reservoir.

The release of phosphorus (P) from crustal rocks during weathering plays a key role in determining the size of Earth's biosphere, yet the concentration of P in crustal rocks over time remains controversial. Here, we combine spatial, temporal, and chemical measurements of preserved rocks to reconstruct the lithological and chemical evolution of Earth's continental crust. We identify a threefold increase in average crustal P concentrations across the Neoproterozoic-Phanerozoic boundary (600 to 400 million years), showing that preferential biomass burial on shelves acted to progressively concentrate P within continental crust. Rapid compositional change was made possible by massive removal of ancient P-poor rock and deposition of young P-rich sediment during an episode of enhanced global erosion. Subsequent weathering of newly P-rich crust led to increased riverine P fluxes to the ocean. Our results suggest that global erosion coupled to sedimentary P-enrichment forged a markedly nutrient-rich crust at the dawn of the Phanerozoic.

Nitrogen Cycling and Biosignatures in a Hyperarid Mars Analog Environment.

The hyperarid Atacama Desert is a unique Mars-analog environment with a large near-surface soil nitrate reservoir due to the lack of rainfall leaching for millennia. We investigated nitrogen (N) cycling and organic matter dynamics in this nitrate-rich terrestrial environment by analyzing the concentrations and isotopic compositions of nitrate, organic C, and organic N, coupled with microbial pathway-enzyme inferences, across a naturally occurring rainfall gradient. Nitrate deposits in sites with an annual precipitation of <10 mm carry atmospheric δ15N, δ18O, and Δ17O signatures, while these values are overprinted by biological cycling in sites with >15 mm annual precipitation. Metagenomic analyses suggest that the Atacama Desert harbors a unique biological nitrogen cycle driven by nitrifier denitrification, nitric oxide dioxygenase-driven alternative nitrification, and organic N loss pathways. Nitrate assimilation is the only nitrate consumption pathway available in the driest sites, although some hyperarid sites also support organisms with ammonia lyase- and nitric oxide synthase-driven organic N loss. Nitrifier denitrification is enhanced in the "transition zone" desert environments, which are generally hyperarid but see occasional large rainfall events, and shifts to nitric oxide dioxygenase-driven alternative nitrifications in wetter arid sites. Since extremophilic microorganisms tend to exploit all reachable nutrients, both N and O isotope fractionations during N transformations are reduced. These results suggest that N cycling on the more recent dry Mars might be dominated by nitrate assimilation that cycles atmospheric nitrate and exchanges water O during intermittent wetting, resulting stable isotope biosignatures could shift away from martian atmospheric nitrate endmember. Early wetter Mars could nurture putative life that metabolized nitrate with traceable paleoenvironmental isotopic markers similar to microbial denitrification and nitrification stored in deep subsurface.

Sulfur isotopes of hydrothermal vent fossils and insights into microbial sulfur cycling within a lower Paleozoic (Ordovician-early Silurian) vent community.

Symbioses between metazoans and microbes involved in sulfur cycling are integral to the ability of animals to thrive within deep-sea hydrothermal vent environments; the development of such interactions is regarded as a key adaptation in enabling animals to successfully colonize vents. Microbes often colonize the surfaces of vent animals and, remarkably, these associations can also be observed intricately preserved by pyrite in the fossil record of vent environments, stretching back to the lower Paleozoic (Ordovician-early Silurian). In non-vent environments, sulfur isotopes are often employed to investigate the metabolic strategies of both modern and fossil organisms, as certain metabolic pathways of microbes, notably sulfate reduction, can produce large sulfur isotope fractionations. However, the sulfur isotopes of vent fossils, both ancient and recently mineralized, have seldom been explored, and it is not known if the pyrite-preserved vent organisms might also preserve potential signatures of their metabolisms. Here, we use high-resolution secondary ion mass spectrometry (SIMS) to investigate the sulfur isotopes of pyrites from recently mineralized and Ordovician-early Silurian tubeworm fossils with associated microbial fossils. Our results demonstrate that pyrites containing microbial fossils consistently have significantly more negative δ34 S values compared with nearby non-fossiliferous pyrites, and thus represent the first indication that the presence of microbial sulfur-cycling communities active at the time of pyrite formation influenced the sulfur isotope signatures of pyrite at hydrothermal vents. The observed depletions in δ34 S are generally small in magnitude and are perhaps best explained by sulfur isotope fractionation through a combination of sulfur-cycling processes carried out by vent microbes. These results highlight the potential for using sulfur isotopes to explore biological functional relationships within fossil vent communities, and to enhance understanding of how microbial and animal life has co-evolved to colonize vents throughout geological time.

Geological constraints on the origin of oxygenic photosynthesis.

This article examines the geological evidence for the rise of atmospheric oxygen and the origin of oxygenic photosynthesis. The evidence for the rise of atmospheric oxygen places a minimum time constraint before which oxygenic photosynthesis must have developed, and was subsequently established as the primary control on the atmospheric oxygen level. The geological evidence places the global rise of atmospheric oxygen, termed the Great Oxidation Event (GOE), between ~2.45 and ~2.32 Ga, and it is captured within the Duitschland Formation, which shows a transition from mass-independent to mass-dependent sulfur isotope fractionation. The rise of atmospheric oxygen during this interval is closely associated with a number of environmental changes, such as glaciations and intense continental weathering, and led to dramatic changes in the oxidation state of the ocean and the seawater inventory of transition elements. There are other features of the geologic record predating the GOE by as much as 200-300 million years, perhaps extending as far back as the Mesoarchean-Neoarchean boundary at 2.8 Ga, that suggest the presence of low level, transient or local, oxygenation. If verified, these features would not only imply an earlier origin for oxygenic photosynthesis, but also require a mechanism to decouple oxygen production from oxidation of Earth's surface environments. Most hypotheses for the GOE suggest that oxygen production by oxygenic photosynthesis is a precondition for the rise of oxygen, but that a synchronous change in atmospheric oxygen level is not required by the onset of this oxygen source. The potential lag-time in the response of Earth surface environments is related to the way that oxygen sinks, such as reduced Fe and sulfur compounds, respond to oxygen production. Changes in oxygen level imply an imbalance in the sources and sinks for oxygen. Changes in the cycling of oxygen have occurred at various times before and after the GOE, and do not appear to require corresponding changes in the intensity of oxygenic photosynthesis. The available geological constraints for these changes do not, however, disallow a direct role for this metabolism. The geological evidence for early oxygen and hypotheses for the controls on oxygen level are the basis for the interpretation of photosynthetic oxygen production as examined in this review.

Volcanic controls on the microbial habitability of Mars-analogue hydrothermal environments.

Due to their potential to support chemolithotrophic life, relic hydrothermal systems on Mars are a key target for astrobiological exploration. We analysed water and sediments at six geothermal pools from the rhyolitic Kerlingarfjöll and basaltic Kverkfjöll volcanoes in Iceland, to investigate the localised controls on the habitability of these systems in terms of microbial community function. Our results show that host lithology plays a minor role in pool geochemistry and authigenic mineralogy, with the system geochemistry primarily controlled by deep volcanic processes. We find that by dictating pool water pH and redox conditions, deep volcanic processes are the primary control on microbial community structure and function, with water input from the proximal glacier acting as a secondary control by regulating pool temperatures. Kerlingarfjöll pools have reduced, circum-neutral CO2 -rich waters with authigenic calcite-, pyrite- and kaolinite-bearing sediments. The dominant metabolisms inferred from community profiles obtained by 16S rRNA gene sequencing are methanogenesis, respiration of sulphate and sulphur (S0 ) oxidation. In contrast, Kverkfjöll pools have oxidised, acidic (pH < 3) waters with high concentrations of SO42- and high argillic alteration, resulting in Al-phyllosilicate-rich sediments. The prevailing metabolisms here are iron oxidation, sulphur oxidation and nitrification. Where analogous ice-fed hydrothermal systems existed on early Mars, similar volcanic processes would likely have controlled localised metabolic potential and thus habitability. Moreover, such systems offer several habitability advantages, including a localised source of metabolic redox pairs for chemolithotrophic microorganisms and accessible trace metals. Similar pools could have provided transient environments for life on Mars; when paired with surface or near-surface ice, these habitability niches could have persisted into the Amazonian. Additionally, they offer a confined site for biosignature formation and deposition that lends itself well to in situ robotic exploration.

Unraveling biogeochemical phosphorus dynamics in hyperarid Mars-analogue soils using stable oxygen isotopes in phosphate.

With annual precipitation less than 20 mm and extreme UV intensity, the Atacama Desert in northern Chile has long been utilized as an analogue for recent Mars. In these hyperarid environments, water and biomass are extremely limited, and thus, it becomes difficult to generate a full picture of biogeochemical phosphate-water dynamics. To address this problem, we sampled soils from five Atacama study sites and conducted three main analyses-stable oxygen isotopes in phosphate, enzyme pathway predictions, and cell culture experiments. We found that high sedimentation rates decrease the relative size of the organic phosphorus pool, which appears to hinder extremophiles. Phosphoenzyme and pathway prediction analyses imply that inorganic pyrophosphatase is the most likely catalytic agent to cycle P in these environments, and this process will rapidly overtake other P utilization strategies. In these soils, the biogenic δ18 O signatures of the soil phosphate (δ18 OPO4 ) can slowly overprint lithogenic δ18 OPO4 values over a timescale of tens to hundreds of millions of years when annual precipitation is more than 10 mm. The δ18 OPO4 of calcium-bound phosphate minerals seems to preserve the δ18 O signature of the water used for biogeochemical P cycling, pointing toward sporadic rainfall and gypsum hydration water as key moisture sources. Where precipitation is less than 2 mm, biological cycling is restricted and bedrock δ18 OPO4 values are preserved. This study demonstrates the utility of δ18 OPO4 values as indicative of biogeochemical cycling and hydrodynamics in an extremely dry Mars-analogue environment.

Anomalous fractionation of mercury isotopes in the Late Archean atmosphere.

Earth's surface underwent a dramatic transition ~2.3 billion years ago when atmospheric oxygen first accumulated during the Great Oxidation Event, but the detailed composition of the reducing early atmosphere is not well known. Here we develop mercury (Hg) stable isotopes as a proxy for paleoatmospheric chemistry and use Hg isotope data from 2.5 billion-year-old sedimentary rocks to examine changes in the Late Archean atmosphere immediately prior to the Great Oxidation Event. These sediments preserve evidence of strong photochemical transformations of mercury in the absence of molecular oxygen. In addition, these geochemical records combined with previously published multi-proxy data support a vital role for methane in Earth's early atmosphere.

Nitrates as a Potential N Supply for Microbial Ecosystems in a Hyperarid Mars Analog System.

Nitrate is common in Mars sediments owing to long-term atmospheric photolysis, oxidation, and potentially, impact shock heating. The Atacama Desert in Chile, which is the driest region on Earth and rich in nitrate deposits, is used as a Mars analog in this study to explore the potential effects of high nitrate levels on growth of extremophilic ecosystems. Seven study sites sampled across an aridity gradient in the Atacama Desert were categorized into 3 clusters-hyperarid, middle, and arid sites-as defined by essential soil physical and chemical properties. Intriguingly, the distribution of nitrate concentrations in the shallow subsurface suggests that the buildup of nitrate is not solely controlled by precipitation. Correlations of nitrate with SiO2/Al2O3 and grain sizes suggest that sedimentation rates may also be important in controlling nitrate distribution. At arid sites receiving more than 10 mm/yr precipitation, rainfall shows a stronger impact on biomass than nitrate does. However, high nitrate to organic carbon ratios are generally beneficial to N assimilation, as evidenced both by soil geochemistry and enriched culturing experiments. This study suggests that even in the absence of precipitation, nitrate levels on a more recent, hyperarid Mars could be sufficiently high to benefit potentially extant Martian microorganisms.

Sulfate was a trace constituent of Archean seawater.

In the low-oxygen Archean world (>2400 million years ago), seawater sulfate concentrations were much lower than today, yet open questions frustrate the translation of modern measurements of sulfur isotope fractionations into estimates of Archean seawater sulfate concentrations. In the water column of Lake Matano, Indonesia, a low-sulfate analog for the Archean ocean, we find large (>20 per mil) sulfur isotope fractionations between sulfate and sulfide, but the underlying sediment sulfides preserve a muted range of δ(34)S values. Using models informed by sulfur cycling in Lake Matano, we infer Archean seawater sulfate concentrations of less than 2.5 micromolar. At these low concentrations, marine sulfate residence times were likely 10(3) to 10(4) years, and sulfate scarcity would have shaped early global biogeochemical cycles, possibly restricting biological productivity in Archean oceans.

Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces.

Distinct partitioning has been observed in the composition and diversity of bacterial communities inhabiting the surface and overlying seawater of three coral species infected with black band disease (BBD) on the southern Caribbean island of Curaçao, Netherlands Antilles. PCR amplification and sequencing of bacterial 16S rRNA genes (rDNA) with universally conserved primers have identified over 524 unique bacterial sequences affiliated with 12 bacterial divisions. The molecular sequences exhibited less than 5% similarity in bacterial community composition between seawater and the healthy, black band diseased, and dead coral surfaces. The BBD bacterial mat rapidly migrates across and kills the coral tissue. Clone libraries constructed from the BBD mat were comprised of eight bacterial divisions and 13% unknowns. Several sequences representing bacteria previously found in other marine and terrestrial organisms (including humans) were isolated from the infected coral surfaces, including Clostridium spp., Arcobacter spp., Campylobacter spp., Cytophaga fermentans, Cytophaga columnaris, and Trichodesmium tenue.