Co-evolution of early Earth environments and microbial life.

Two records of Earth history capture the evolution of life and its co-evolving ecosystems with interpretable fidelity: the geobiological and geochemical traces preserved in rocks and the evolutionary histories captured within genomes. The earliest vestiges of life are recognized mostly in isotopic fingerprints of specific microbial metabolisms, whereas fossils and organic biomarkers become important later. Molecular biology provides lineages that can be overlayed on geologic and geochemical records of evolving life. All these data lie within a framework of biospheric evolution that is primarily characterized by the transition from an oxygen-poor to an oxygen-rich world. In this Review, we explore the history of microbial life on Earth and the degree to which it shaped, and was shaped by, fundamental transitions in the chemical properties of the oceans, continents and atmosphere. We examine the diversity and evolution of early metabolic processes, their couplings with biogeochemical cycles and their links to the oxygenation of the early biosphere. We discuss the distinction between the beginnings of metabolisms and their subsequent proliferation and their capacity to shape surface environments on a planetary scale. The evolution of microbial life and its ecological impacts directly mirror the Earth's chemical and physical evolution through cause-and-effect relationships.

Transient fertilization of a post-Sturtian Snowball ocean margin with dissolved phosphate by clay minerals.

Marine sedimentary rocks deposited across the Neoproterozoic Cryogenian Snowball interval, ~720-635 million years ago, suggest that post-Snowball fertilization of shallow continental margin seawater with phosphorus accelerated marine primary productivity, ocean-atmosphere oxygenation, and ultimately the rise of animals. However, the mechanisms that sourced and delivered bioavailable phosphate from land to the ocean are not fully understood. Here we demonstrate a causal relationship between clay mineral production by the melting Sturtian Snowball ice sheets and a short-lived increase in seawater phosphate bioavailability by at least 20-fold and oxygenation of an immediate post-Sturtian Snowball ocean margin. Bulk primary sediment inputs and inferred dissolved seawater phosphate dynamics point to a relatively low marine phosphate inventory that limited marine primary productivity and seawater oxygenation before the Sturtian glaciation, and again in the later stages of the succeeding interglacial greenhouse interval.

Are Large Sulfur Isotope Variations Biosignatures in an Ancient, Impact-Induced Hydrothermal Mars Analog?

Discrepancies have emerged concerning the application of sulfur stable isotope ratios as a biosignature in impact crater paleolakes. The first in situ δ34S data from Mars at Gale crater display a ∼75‰ range that has been attributed to an abiotic mechanism. Yet biogeochemical studies of ancient environments on Earth generally interpret δ34S fractionations >21‰ as indicative of a biological origin, and studies of δ34S at analog impact crater lakes on Earth have followed the same approach. We performed analyses (including δ34S, total organic carbon wt%, and scanning electron microscope imaging) on multiple lithologies from the Nördlinger Ries impact crater, focusing on hydrothermally altered impact breccias and associated sedimentary lake-fill sequences to determine whether the δ34S properties define a biosignature. The differences in δ34S between the host lithologies may have resulted from thermochemical sulfate reduction, microbial sulfate reduction, hydrothermal equilibrium fractionation, or any combination thereof. Despite abundant samples and instrumental precision currently exclusive to Earth-bound analyses, assertions of biogenicity from δ34S variations >21‰ at the Miocene Ries impact crater are tenuous. This discourages the use of δ34S as a biosignature in similar environments without independent checks that include the full geologic, biogeochemical, and textural context, as well as a comprehensive acknowledgment of alternative hypotheses.

Uncovering the Ediacaran phosphorus cycle.

Phosphorus is a limiting nutrient that is thought to control oceanic oxygen levels to a large extent1-3. A possible increase in marine phosphorus concentrations during the Ediacaran Period (about 635-539 million years ago) has been proposed as a driver for increasing oxygen levels4-6. However, little is known about the nature and evolution of phosphorus cycling during this time4. Here we use carbonate-associated phosphate (CAP) from six globally distributed sections to reconstruct oceanic phosphorus concentrations during a large negative carbon-isotope excursion-the Shuram excursion (SE)-which co-occurred with global oceanic oxygenation7-9. Our data suggest pulsed increases in oceanic phosphorus concentrations during the falling and rising limbs of the SE. Using a quantitative biogeochemical model, we propose that this observation could be explained by carbon dioxide and phosphorus release from marine organic-matter oxidation primarily by sulfate, with further phosphorus release from carbon-dioxide-driven weathering on land. Collectively, this may have resulted in elevated organic-pyrite burial and ocean oxygenation. Our CAP data also seem to suggest equivalent oceanic phosphorus concentrations under maximum and minimum extents of ocean anoxia across the SE. This observation may reflect decoupled phosphorus and ocean anoxia cycles, as opposed to their coupled nature in the modern ocean. Our findings point to external stimuli such as sulfate weathering rather than internal oceanic phosphorus-oxygen cycling alone as a possible control on oceanic oxygenation in the Ediacaran. In turn, this may help explain the prolonged rise of atmospheric oxygen levels.

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

Many lines of inorganic geochemical evidence suggest transient "whiffs" of environmental oxygenation before the Great Oxidation Event (GOE). Slotznick et al. assert that analyses of paleoredox proxies in the Mount McRae Shale, Western Australia, were misinterpreted and hence that environmental O2 levels were persistently negligible before the GOE. We find these arguments logically flawed and factually incomplete.

Reconstructing Earth's atmospheric oxygenation history using machine learning.

Reconstructing historical atmospheric oxygen (O2) levels at finer temporal resolution is a top priority for exploring the evolution of life on Earth. This goal, however, is challenged by gaps in traditionally employed sediment-hosted geochemical proxy data. Here, we propose an independent strategy-machine learning with global mafic igneous geochemistry big data to explore atmospheric oxygenation over the last 4.0 billion years. We observe an overall two-step rise of atmospheric O2 similar to the published curves derived from independent sediment-hosted paleo-oxybarometers but with a more detailed fabric of O2 fluctuations superimposed. These additional, shorter-term fluctuations are also consistent with previous but less well-established suggestions of O2 variability. We conclude from this agreement that Earth's oxygenated atmosphere may therefore be at least partly a natural consequence of mantle cooling and specifically that evolving mantle melts collectively have helped modulate the balance of early O2 sources and sinks.

Frontiers in Prebiotic Chemistry and Early Earth Environments.

The Prebiotic Chemistry and Early Earth Environments (PCE3) Consortium is a community of researchers seeking to understand the origins of life on Earth and in the universe. PCE3 is one of five Research Coordination Networks (RCNs) within NASA's Astrobiology Program. Here we report on the inaugural PCE3 workshop, intended to cross-pollinate, transfer information, promote cooperation, break down disciplinary barriers, identify new directions, and foster collaborations. This workshop, entitled, "Building a New Foundation", was designed to propagate current knowledge, identify possibilities for multidisciplinary collaboration, and ultimately define paths for future collaborations. Presentations addressed the likely conditions on early Earth in ways that could be incorporated into prebiotic chemistry experiments and conceptual models to improve their plausibility and accuracy. Additionally, the discussions that followed among workshop participants helped to identify within each subdiscipline particularly impactful new research directions. At its core, the foundational knowledge base presented in this workshop should underpin future workshops and enable collaborations that bridge the many disciplines that are part of PCE3.

Strong evidence for a weakly oxygenated ocean-atmosphere system during the Proterozoic.

Earth's surface has undergone a protracted oxygenation, which is commonly assumed to have profoundly affected the biosphere. However, basic aspects of this history are still debated-foremost oxygen (O2) levels in the oceans and atmosphere during the billion years leading up to the rise of algae and animals. Here we use isotope ratios of iron (Fe) in ironstones-Fe-rich sedimentary rocks deposited in nearshore marine settings-as a proxy for O2 levels in shallow seawater. We show that partial oxidation of dissolved Fe(II) was characteristic of Proterozoic shallow marine environments, whereas younger ironstones formed via complete oxidation of Fe(II). Regardless of the Fe(II) source, partial Fe(II) oxidation requires low O2 in the shallow oceans, settings crucial to eukaryotic evolution. Low O2 in surface waters can be linked to markedly low atmospheric O2-likely requiring less than 1% of modern levels. Based on our records, these conditions persisted (at least periodically) until a shift toward higher surface O2 levels between ca 900 and 750 Ma, coincident with an apparent rise in eukaryotic ecosystem complexity. This supports the case that a first-order shift in surface O2 levels during this interval may have selected for life modes adapted to more oxygenated habitats.

Proterozoic supercontinent break-up as a driver for oxygenation events and subsequent carbon isotope excursions.

Oxygen and carbon are 2 elements critical for life on Earth. Earth's most dramatic oxygenation events and carbon isotope excursions (CIE) occurred during the Proterozoic, including the Paleoproterozoic Great Oxidation Event and the associated Lomagundi CIE, the Neoproterozoic Oxygenation event, and the Shuram negative CIE during the late Neoproterozoic. A specific pattern of a long-lived positive CIE followed by a negative CIE is observed in association with oxygenation events during the Paleo- and Neo-proterozoic. We present results from a carbon cycle model designed to couple the surface and interior cycling of carbon that reproduce this pattern. The model assumes organic carbon resides in the mantle longer than carbonate, leading to systematic temporal variations in the δ13C of volcanic CO2 emissions. When the model is perturbed by periods of enhanced continental weathering, increased amounts of carbonate and organic carbon are buried. Increased deposition of organic carbon allows O2 accumulation, while positive CIEs are driven by rapid release of subducted carbonate-derived CO2 at arcs. The subsequent negative CIEs are driven by the delayed release of organic C-derived CO2 at ocean islands. Our model reproduces the sequences observed in the Paleo- and Neo-proterozoic, that is oxygenation accompanied by a positive CIE followed by a negative CIE. Periods of enhanced weathering correspond temporally to supercontinent break-up, suggesting an important connection between global tectonics and the evolution of oxygen and carbon on Earth.

Reconciling evidence of oxidative weathering and atmospheric anoxia on Archean Earth.

Evidence continues to emerge for the production and low-level accumulation of molecular oxygen (O2) at Earth's surface before the Great Oxidation Event. Quantifying this early O2 has proven difficult. Here, we use the distribution and isotopic composition of molybdenum in the ancient sedimentary record to quantify Archean Mo cycling, which allows us to calculate lower limits for atmospheric O2 partial pressures (PO2) and O2 production fluxes during the Archean. We consider two end-member scenarios. First, if O2 was evenly distributed throughout the atmosphere, then PO2 > 10­6.9 present atmospheric level was required for large periods of time during the Archean eon. Alternatively, if O2 accumulation was instead spatially restricted (e.g., occurring only near the sites of O2 production), then O2 production fluxes >0.01 Tmol O2/year were required. Archean O2 levels were vanishingly low according to our calculations but substantially above those predicted for an abiotic Earth system.

Introduction-First Billion Years: Habitability.

The physical processes active during the first billion years (FBY) of Earth's history, such as accretion, differentiation, and impact cratering, provide constraints on the initial conditions that were conducive to the formation and establishment of life on Earth. This motivated the Lunar and Planetary Institute's FBY topical initiative, which was a four-part conference series intended to look at each of these physical processes to study the basic structure and composition of our Solar System that was set during the FBY. The FBY Habitability conference, held in September 2019, was the last in this series and was intended to synthesize the initiative; specifically, to further our understanding of the origins of life, planetary and environmental habitability, and the search for life beyond Earth. The conference included discussions of planetary habitability and the potential emergence of life on bodies within our Solar System, as well as extrasolar systems by applying our knowledge of the Solar System's FBY, and in particular Earth's early history. To introduce this Special Collection, which resulted from work discussed at the conference, we provide a review of the main themes and a synopsis of the FBY Habitability conference.

Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview.

The long history of life on Earth has unfolded as a cause-and-effect relationship with the evolving amount of oxygen (O2) in the oceans and atmosphere. Oxygen deficiency characterized our planet's first 2 billion years, yet evidence for biological O2 production and local enrichments in the surface ocean appear long before the first accumulations of O2 in the atmosphere roughly 2.4 to 2.3 billion years ago. Much has been written about this fundamental transition and the related balance between biological O2 production and sinks coupled to deep Earth processes that could buffer against the accumulation of biogenic O2. However, the relationship between complex life (eukaryotes, including animals) and later oxygenation is less clear. Some data suggest O2 was higher but still mostly low for another billion and a half years before increasing again around 800 million years ago, potentially setting a challenging course for complex life during its initial development and ecological expansion. The apparent rise in O2 around 800 million years ago is coincident with major developments in complex life. Multiple geochemical and paleontological records point to a major biogeochemical transition at that time, but whether rising and still dynamic biospheric oxygen triggered or merely followed from innovations in eukaryotic ecology, including the emergence of animals, is still debated. This paper focuses on the geochemical records of Earth's middle history, roughly 1.8 to 0.5 billion years ago, as a backdrop for exploring possible cause-and-effect relationships with biological evolution and the primary controls that may have set its pace, including solid Earth/tectonic processes, nutrient limitation, and their possible linkages. A richer mechanistic understanding of the interplay between coevolving life and Earth surface environments can provide a template for understanding and remotely searching for sustained habitability and even life on distant exoplanets.

Massive formation of early diagenetic dolomite in the Ediacaran ocean: Constraints on the "dolomite problem".

Paleozoic and Precambrian sedimentary successions frequently contain massive dolomicrite [CaMg(CO3)2] units despite kinetic inhibitions to nucleation and precipitation of dolomite at Earth surface temperatures (<60 °C). This paradoxical observation is known as the "dolomite problem." Accordingly, the genesis of these dolostones is usually attributed to burial-hydrothermal dolomitization of primary limestones (CaCO3) at temperatures of >100 °C, thus raising doubt about the validity of these deposits as archives of Earth surface environments. We present a high-resolution, >63-My-long clumped-isotope temperature (TΔ47) record of shallow-marine dolomicrites from two drillcores of the Ediacaran (635 to 541 Ma) Doushantuo Formation in South China. Our T∆47 record indicates that a majority (87%) of these dolostones formed at temperatures of <100 °C. When considering the regional thermal history, modeling of the influence of solid-state reordering on our TΔ47 record further suggests that most of the studied dolostones formed at temperatures of <60 °C, providing direct evidence of a low-temperature origin of these dolostones. Furthermore, calculated δ18O values of diagenetic fluids, rare earth element plus yttrium compositions, and petrographic observations of these dolostones are consistent with an early diagenetic origin in a rock-buffered environment. We thus propose that a precursor precipitate from seawater was subsequently dolomitized during early diagenesis in a near-surface setting to produce the large volume of dolostones in the Doushantuo Formation. Our findings suggest that the preponderance of dolomite in Paleozoic and Precambrian deposits likely reflects oceanic conditions specific to those eras and that dolostones can be faithful recorders of environmental conditions in the early oceans.

Nitrogen isotope ratios trace high-pH conditions in a terrestrial Mars analog site.

High-pH alkaline lakes are among the most productive ecosystems on Earth and prime targets in the search for life on Mars; however, a robust proxy for such settings does not yet exist. Nitrogen isotope fractionation resulting from NH3 volatilization at high pH has the potential to fill this gap. To validate this idea, we analyzed samples from the Nördlinger Ries, a Miocene impact crater lake that displayed pH values up to 9.8 as inferred from mineralogy and aqueous modeling. Our data show a peak in δ15N of +17‰ in the most alkaline facies, followed by a gradual decline to around +5‰, concurrent with the proposed decline in pH, highlighting the utility of nitrogen isotopes as a proxy for high-pH conditions. In combination with independent mineralogical indicators for high alkalinity, nitrogen isotopes can provide much-needed quantitative constraints on ancient atmospheric Pco2 (partial pressure of CO2) and thus climatic controls on early Earth and Mars.

Correlation between biomarkers of exposure, effect and potential harm in the urine of electronic cigarette users.

OBJECTIVES: To determine if urinary biomarkers of effect and potential harm are elevated in electronic cigarette users compared with non-smokers and if elevation correlates with increased concentrations of metals in urine. STUDY DESIGN AND SETTING: This was a cross-sectional study of biomarkers of exposure, effect and potential harm in urine from non-smokers (n=20), electronic cigarette users (n=20) and cigarette smokers (n=13). Participant's screening and urine collection were performed at the Roswell Park Comprehensive Cancer Center, and biomarker analysis and metal analysis were performed at the University of California, Riverside. RESULTS: Metallothionein was significantly elevated in the electronic cigarette group (3761±3932 pg/mg) compared with the non-smokers (1129±1294 pg/mg, p=0.05). 8-OHdG (8-hydroxy-2'-deoxyguanosine) was significantly elevated in electronic cigarette users (442.8±300.7 ng/mg) versus non-smokers (221.6±157.8 ng/mg, p=0.01). 8-Isoprostane showed a significant increase in electronic cigarette users (750.8±433 pg/mg) versus non-smokers (411.2±287.4 pg/mg, p=0.03). Linear regression analysis in the electronic cigarette group showed a significant correlation between cotinine and total metal concentration; total metal concentration and metallothionein; cotinine and oxidative DNA damage; and total metal concentration and oxidative DNA damage. Zinc was significantly elevated in the electronic cigarette users (584.5±826.6 µg/g) compared with non-smokers (413.6±233.7 µg/g, p=0.03). Linear regression analysis showed a significant correlation between urinary zinc concentration and 8-OHdG in the electronic cigarette users. CONCLUSIONS: This study is the first to investigate biomarkers of potential harm and effect in electronic cigarette users and to show a linkage to metal exposure. The biomarker levels in electronic cigarette users were similar to (and not lower than) cigarette smokers. In electronic cigarette users, there was a link to elevated total metal exposure and oxidative DNA damage. Specifically, our results demonstrate that zinc concentration was correlated to oxidative DNA damage.

Absence of biomarker evidence for early eukaryotic life from the Mesoproterozoic Roper Group: Searching across a marine redox gradient in mid-Proterozoic habitability.

By about 2.0 billion years ago (Ga), there is evidence for a period best known for its extended, apparent geochemical stability expressed famously in the carbonate-carbon isotope data. Despite the first appearance and early innovation among eukaryotic organisms, this period is also known for a rarity of eukaryotic fossils and an absence of organic biomarker fingerprints for those organisms, suggesting low diversity and relatively small populations compared to the Neoproterozoic era. Nevertheless, the search for diagnostic biomarkers has not been performed with guidance from paleoenvironmental redox constrains from inorganic geochemistry that should reveal the facies that were most likely hospitable to these organisms. Siltstones and shales obtained from drill core of the ca. 1.3-1.4 Ga Roper Group from the McArthur Basin of northern Australia provide one of our best windows into the mid-Proterozoic redox landscape. The group is well dated and minimally metamorphosed (of oil window maturity), and previous geochemical data suggest a relatively strong connection to the open ocean compared to other mid-Proterozoic records. Here, we present one of the first integrated investigations of Mesoproterozoic biomarker records performed in parallel with established inorganic redox proxy indicators. Results reveal a temporally variable paleoredox structure through the Velkerri Formation as gauged from iron mineral speciation and trace-metal geochemistry, vacillating between oxic and anoxic. Our combined lipid biomarker and inorganic geochemical records indicate at least episodic euxinic conditions sustained predominantly below the photic zone during the deposition of organic-rich shales found in the middle Velkerri Formation. The most striking result is an absence of eukaryotic steranes (4-desmethylsteranes) and only traces of gammacerane in some samples-despite our search across oxic, as well as anoxic, facies that should favor eukaryotic habitability and in low maturity rocks that allow the preservation of biomarker alkanes. The dearth of Mesoproterozoic eukaryotic sterane biomarkers, even within the more oxic facies, is somewhat surprising but suggests that controls such as the long-term nutrient balance and other environmental factors may have throttled the abundances and diversity of early eukaryotic life relative to bacteria within marine microbial communities. Given that molecular clocks predict that sterol synthesis evolved early in eukaryotic history, and (bacterial) fossil steroids have been found previously in 1.64 Ga rocks, then a very low environmental abundance of eukaryotes relative to bacteria is our preferred explanation for the lack of regular steranes and only traces of gammacerane in a few samples. It is also possible that early eukaryotes adapted to Mesoproterozoic marine environments did not make abundant steroid lipids or tetrahymanol in their cell membranes.

Nitrous oxide from chemodenitrification: A possible missing link in the Proterozoic greenhouse and the evolution of aerobic respiration.

The potent greenhouse gas nitrous oxide (N2 O) may have been an important constituent of Earth's atmosphere during Proterozoic (~2.5-0.5 Ga). Here, we tested the hypothesis that chemodenitrification, the rapid reduction of nitric oxide by ferrous iron, would have enhanced the flux of N2 O from ferruginous Proterozoic seas. We empirically derived a rate law, d N 2 O d t = 7.2 × 10 - 5 [ Fe 2 + ] 0.3 [ NO ] 1 , and measured an isotopic site preference of +16‰ for the reaction. Using this empirical rate law, and integrating across an oceanwide oxycline, we found that low nM NO and µM-low mM Fe2+ concentrations could have sustained a sea-air flux of 100-200 Tg N2 O-N year-1 , if N2 fixation rates were near-modern and all fixed N2 was emitted as N2 O. A 1D photochemical model was used to obtain steady-state atmospheric N2 O concentrations as a function of sea-air N2 O flux across the wide range of possible pO2 values (0.001-1 PAL). At 100-200 Tg N2 O-N year-1 and >0.1 PAL O2 , this model yielded low-ppmv N2 O, which would produce several degrees of greenhouse warming at 1.6 ppmv CH4 and 320 ppmv CO2 . These results suggest that enhanced N2 O production in ferruginous seawater via a previously unconsidered chemodenitrification pathway may have helped to fill a Proterozoic "greenhouse gap," reconciling an ice-free Mesoproterozoic Earth with a less luminous early Sun. A particularly notable result was that high N2 O fluxes at intermediate O2 concentrations (0.01-0.1 PAL) would have enhanced ozone screening of solar UV radiation. Due to rapid photolysis in the absence of an ozone shield, N2 O is unlikely to have been an important greenhouse gas if Mesoproterozoic O2 was 0.001 PAL. At low O2 , N2 O might have played a more important role as life's primary terminal electron acceptor during the transition from an anoxic to oxic surface Earth, and correspondingly, from anaerobic to aerobic metabolisms.

Late inception of a resiliently oxygenated upper ocean.

Rising oceanic and atmospheric oxygen levels through time have been crucial to enhanced habitability of surface Earth environments. Few redox proxies can track secular variations in dissolved oxygen concentrations around threshold levels for metazoan survival in the upper ocean. We present an extensive compilation of iodine-to-calcium ratios (I/Ca) in marine carbonates. Our record supports a major rise in the partial pressure of oxygen in the atmosphere at ~400 million years (Ma) ago and reveals a step change in the oxygenation of the upper ocean to relatively sustainable near-modern conditions at ~200 Ma ago. An Earth system model demonstrates that a shift in organic matter remineralization to greater depths, which may have been due to increasing size and biomineralization of eukaryotic plankton, likely drove the I/Ca signals at ~200 Ma ago.