Metal limitation of cyanobacterial N2 fixation and implications for the Precambrian nitrogen cycle

Nitrogen fixation is a critical part of the global nitrogen cycle, replacing biologically available reduced nitrogen lost by denitrification. The redox‐sensitive trace metals Fe and Mo are key components of the primary nitrogenase enzyme used by cyanobacteria (and other prokaryotes) to fix atmospheric N₂ into bioessential compounds. Progressive oxygenation of the Earth's atmosphere has forced changes in the redox state of the oceans through geologic time, from anoxic Fe‐enriched waters in the Archean to partially sulfidic deep waters by the mid‐Proterozoic. This development of ocean redox chemistry during the Precambrian led to fluctuations in Fe and Mo availability that could have significantly impacted the ability of prokaryotes to fix nitrogen. It has been suggested that metal limitation of nitrogen fixation and nitrate assimilation, along with increased rates of denitrification, could have resulted in globally reduced rates of primary production and nitrogen‐starved oceans through much of the Proterozoic. To test the first part of this hypothesis, we grew N₂‐fixing cyanobacteria in cultures with metal concentrations reflecting an anoxic Archean ocean (high Fe, low Mo), a sulfidic Proterozoic ocean (low Fe, moderate Mo), and an oxic Phanerozoic ocean (low Fe, high Mo). We measured low rates of cellular N₂ fixation under [Fe] and [Mo] estimated for the Archean ocean. With decreased [Fe] and higher [Mo] representing sulfidic Proterozoic conditions, N₂ fixation, growth, and biomass C:N were similar to those observed with metal concentrations of the fully oxygenated oceans that likely developed in the Phanerozoic. Our results raise the possibility that an initial rise in atmospheric oxygen could actually have enhanced nitrogen fixation rates to near modern marine levels, providing that phosphate was available and rising O₂ levels did not markedly inhibit nitrogenase activity.     

A paleosol record of the evolution of Cr redox cycling and evidence for an increase in atmospheric oxygen during the Neoproterozoic

Atmospheric oxygen levels control the oxidative side of key biogeochemical cycles and place limits on the development of high‐energy metabolisms. Understanding Earth's oxygenation is thus critical to developing a clearer picture of Earth's long‐term evolution. However, there is currently vigorous debate about even basic aspects of the timing and pattern of the rise of oxygen. Chemical weathering in the terrestrial environment occurs in contact with the atmosphere, making paleosols potentially ideal archives to track the history of atmospheric O₂ levels. Here we present stable chromium isotope data from multiple paleosols that offer snapshots of Earth surface conditions over the last three billion years. The results indicate a secular shift in the oxidative capacity of Earth's surface in the Neoproterozoic and suggest low atmospheric oxygen levels (<1% PAL pO₂) through the majority of Earth's history. The paleosol record also shows that localized Cr oxidation may have begun as early as the Archean, but efficient, modern‐like transport of hexavalent Cr under an O₂‐rich atmosphere did not become common until the Neoproterozoic.     

Biogeochemical modelling of the rise in atmospheric oxygen

Understanding the evolution of atmospheric molecular oxygen levels is a fundamental unsolved problem in Earth's history. We develop a quantitative biogeochemical model that simulates the Palaeoproterozoic transition of the Earth's atmosphere from a weakly reducing state to an O₂‐rich state. The purpose is to gain an insight into factors that plausibly control the timing and rapidity of the oxic transition. The model uses a simplified atmospheric chemistry (parameterized from complex photochemical models) and evolving redox fluxes in the Earth system. We consider time‐dependent fluxes that include organic carbon burial and associated oxygen production, reducing gases from metamorphic and volcanic sources, oxidative weathering, and the escape of hydrogen to space. We find that the oxic transition occurs in a geologically short time when the O₂‐consuming flux of reducing gases falls below the flux of organic carbon burial that produces O₂. A short timescale for the oxic transition is enhanced by a positive feedback due to decreasing destruction of O₂ as stratospheric ozone forms, which is captured in our atmospheric chemistry parameterization. We show that one numerically self‐consistent solution for the rise of O₂ involves a decline in flux of reducing gases driven by irreversible secular oxidation of the crust caused by time‐integrated hydrogen escape to space in the preoxic atmosphere, and that this is compatible with constraints from the geological record. In this model, the timing of the oxic transition is strongly affected by buffers of reduced materials, particularly iron, in the continental crust. An alternative version of the model, where greater fluxes of reduced hydrothermal cations from the Archean seafloor consume O₂, produces a similar history of O₂ and CH₄. When climate and biosphere feedbacks are included in our model of the oxic transition, we find that multiple ‘Snowball Earth’ events are simulated under certain circumstances, as methane collapses and rises repeatedly before reaching a new steady‐state.     

Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide

Rubisco, the most abundant enzyme on the Earth and responsible for all photosynthetic carbon fixation, is often thought of as a highly conserved and sluggish enzyme. Yet, different algal Rubiscos demonstrate a range of kinetic properties hinting at a history of evolution and adaptation. Here, we show that algal Rubisco has indeed evolved adaptively during ancient and distinct geological periods. Using DNA sequences of extant marine algae of the red and Chromista lineage, we define positive selection within the large subunit of Rubisco, encoded by rbcL, to occur basal to the radiation of modern marine groups. This signal of positive selection appears to be responding to changing intracellular concentrations of carbon dioxide (CO(2)) triggered by physiological adaptations to declining atmospheric CO(2). Within the ecologically important Haptophyta (including coccolithophores) and Bacillariophyta (diatoms), positive selection occurred consistently during periods of falling Phanerozoic CO(2) and suggests emergence of carbon-concentrating mechanisms. During the Proterozoic, a strong signal of positive selection after secondary endosymbiosis occurs at the origin of the Chromista lineage (approx. 1.1 Ga), with further positive selection events until 0.41 Ga, implying a significant and continuous decrease in atmospheric CO(2) encompassing the Cryogenian Snowball Earth events. We surmise that positive selection in Rubisco has been caused by declines in atmospheric CO(2) and hence acts as a proxy for ancient atmospheric CO(2).     

Evolution of iron and oxygen biogeochemical cycles during the Precambrian

Iron (Fe) is an essential element for life, and its geochemical cycle is intimately linked to the coupled history of life and Earth's environment. The accumulated geologic records indicate that ferruginous waters existed in the Precambrian oceans not only before the first major rise of atmospheric O₂ levels (Great Oxidation Event; GOE) during the Paleoproterozoic, but also during the rest of the Proterozoic. However, the interactive evolution of the biogeochemical cycles of O₂ and Fe during the Archean–Proterozoic remains ambiguous. Here, we develop a biogeochemical model to investigate the coupled biogeochemical evolution of Fe–O₂–P–C cycles across the GOE. Our model demonstrates that the marine Fe cycle was less sensitive to changes in the production rate of O₂ before the GOE (atmospheric pO₂ < 10⁻⁶ PAL; present atmospheric level). When the P supply rate to the ocean exceeds a certain threshold, the GOE occurs and atmospheric pO₂ rises to ~10⁻³–10⁻¹ PAL. After the GOE, the marine Fe(II) concentration is highly sensitive to atmospheric pO₂, suggesting that the marine redox landscape during the Proterozoic may have fluctuated between ferruginous conditions and anoxic non-ferruginous conditions with sulfidic water masses around continental margins. At a certain threshold value of atmospheric pO₂ of ~0.3% PAL, the primary oxidation pathway of Fe(II) shifts from the activity of Fe(II)-utilizing anoxygenic photoautotrophs in sunlit surface waters to abiotic process in the deep ocean. This is accompanied by a shift in the primary deposition site of Fe(III) hydroxides from the surface ocean to the deep sea, providing a plausible mechanistic explanation for the observed cessation of iron formations during the Proterozoic.     

The loss of mass-independent fractionation in sulfur due to a Palaeoproterozoic collapse of atmospheric methane

We use a 1‐D numerical model to study the atmospheric photochemistry of oxygen, methane, and sulfur after the advent of oxygenic photosynthesis. We assume that mass‐independent fractionation (MIF) of sulfur isotopes – characteristic of the Archean – was best preserved in sediments when insoluble elemental sulfur (S₈) was an important product of atmospheric photochemistry. Efficient S₈ production requires three things: (i) very low levels of tropospheric O₂; (ii) a source of sulfur gases to the atmosphere at least as large as the volcanic SO₂ source today; and (iii) a sufficiently high abundance of methane or other reduced gas. All three requirements must be met. We suggest that the disappearance of a strong MIF sulfur signature at the beginning of the Proterozoic is better explained by the collapse of atmospheric methane, rather than by a failure of volcanism or the rise of oxygen. The photochemical models are consistent in demanding that methane decline before O₂ can rise (although they are silent as to how quickly), and the collapse of a methane greenhouse effect is consistent with the onset of major ice ages immediately following the disappearance of MIF sulfur. We attribute the decline of methane to the growth of the oceanic sulfate pool as indicated by the widening envelope of mass‐dependent sulfur fractionation through the Archean. We find that a given level of biological forcing can support either oxic or anoxic atmospheres, and that the transition between the anoxic state and the oxic state is inhibited by high levels of atmospheric methane. Transition from an oxygen‐poor to an oxygen‐rich atmosphere occurs most easily when methane levels are low, which suggests that the collapse of methane not only caused the end of MIF S and major ice ages, but it may also have enabled the rise of O₂. In this story the early Proterozoic ice ages were ended by the establishment of a stable oxic atmosphere, which protected a renewed methane greenhouse with an ozone shield.     

Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic–Cambrian changes in atmospheric composition

Photosynthetic uptake of inorganic carbon can raise the pH adjacent to cyanobacterial cells, promoting CaCO₃ precipitation. This effect is enhanced by CO₂ concentrating mechanisms that actively transport into cells for carbon fixation. CO₂ concentrating mechanisms presumably developed in response to atmospheric decrease in CO₂ and increase in O₂ over geological timescales. In present‐day cyanobacteria, CO₂ concentrating mechanisms are induced when the atmospheric partial pressure of CO₂ (p_CO2) falls below ～0.4%. Reduction in p_CO2 during the Proterozoic may have had two successive effects on cyanobacterial calcification. First, fall in p_CO2 below ～1% (33 times present atmospheric level, PAL) resulted in lower dissolved inorganic carbon (DIC) concentrations that reduced pH buffering sufficiently for isolated CaCO₃ crystals to begin to nucleate adjacent to cyanobacterial cells. As a result, blooms of planktic cyanobacteria induced precipitated ‘whitings’ of carbonate mud in the water column whose sedimentary accumulation began to dominate carbonate platforms ～1400–1300 Ma. Second, fall in p_CO2 below ～0.4% (10 PAL) induced CO₂‐concentrating mechanisms that further increased pH rise adjacent to cells and promoted in vivo cyanobacterial sheath calcification. Crossing of this second threshold is indicated in the fossil record by the appearance of Girvanella 750–700 Ma. Coeval acquisition of CO₂ concentrating mechanisms by planktic cyanobacteria further stimulated whiting production. These inferences, that p_CO2 fell below ～1%～1400–1300 Ma and below ～0.4% 750–700 Ma, are consistent with empirical and modelled palaeo‐atmosphere estimates. Development of CO₂ concentrating mechanisms was probably temporarily slowed by global cooling ～700–570 Ma that favoured diffusive entry of CO₂ into cells. Lower levels of temperature and DIC at this time would have reduced seawater carbonate saturation state, also hindering cyanobacterial calcification. It is suggested that as Earth emerged from ‘Snowball’ glaciations in the late Neoproterozoic, global warming and O₂ rise reactivated the development of CO₂ concentrating mechanisms. At the same time, rising levels of temperature, calcium ions and DIC increased seawater carbonate saturation state, stimulating widespread cyanobacterial in vivo sheath calcification in the Early Cambrian. This biocalcification event promoted rapid widespread development of calcified cyanobacterial reefs and transformed benthic microbial carbonate fabrics.     

Greenhouse warming by nitrous oxide and methane in the Proterozoic Eon

An anoxic, sulfidic ocean that may have existed during the Proterozoic Eon (0.54-2.4 Ga) would have had limited trace metal abundances because of the low solubility of metal sulfides. The lack of copper, in particular, could have had a significant impact on marine denitrification. Copper is needed for the enzyme that controls the final step of denitrification, from N(2) O to N(2) . Today, only about 5-6% of denitrification results in release of N(2) O. If all denitrification stopped at N(2) O during the Proterozoic, the N(2) O flux could have been 15-20 times higher than today, producing N(2) O concentrations of several ppmv, but only if O(2) levels were relatively high (>0.1 PAL). At lower O(2) levels, N(2) O is rapidly photodissociated. Methane concentrations may also have been elevated during this time, as has been previously suggested. A lack of dissolved O(2) and sulfate in the deep ocean could have produced a high methane flux from marine sediments, as much as 10-20 times today's methane flux from land. The photochemical lifetime of CH(4) increases as more CH(4) is added to the atmosphere, so CH(4) concentrations of up to 100 ppmv are possible during this time. The combined greenhouse effect of CH(4) and N(2) O could have provided up to 10° of warming, thereby keeping the surface warm during the Proterozoic without necessitating high CO(2) levels. A second oxygenation event near the end of the Proterozoic would have resulted in a reduction in both atmospheric N(2) O and CH(4) , perhaps triggering the Neoproterozoic "Snowball Earth" glaciations.     

Archean photoautotrophy: Some alternatives and limits

From the Archean geological record, one can infer that photoautotrophy evolved early in earth history; however, the nature of this photosynthesis — whether it was predominantly bacterial or cyanobacterial — is less clearly understood. General agreement that the earth's atmosphere did not become oxygen rich before the Early Proterozoic era places constraints on theories concerning more ancient biotas. Accommodating this limitation in various ways, different workers have hypothesized (1) that blue-green algae first evolved in the Early Proterozoic; (2) that oxygen producing proto-cyanobacteria existed in the Archean but had no biochemical mechanism for coping with ambient O₂; and (3) that true cyanobacteria flourished in the Archean, but did not oxygenate the atmosphere because of high rates of oxygen consumption caused, in part, by the emanation of reduced gases from widespread Archean volcanoes.Inversion of hypothesis three leads to another, as yet unexplored, alternative. It is possible that physiologically modern blue-green algae existed in Archean times, but had low productivity. Increased rates of primary production in the Early Proterozoic era resulted in the atmospheric transition documented in strata a this age. An answer to the question of wht productivity should have changed from the Archean to the Proterozoic may lie in the differing tectonic frameworks of the two areas. The earliest evidence of widespread, stable, shallow marine platforms is found in Lower Proterozoic sedimentary sequences. In such environments, productivity was, and is, high. In contrast, Archean shallow water environments are often characterized by rapid rates of clastic and pyroclastic influx —conditions that reduced rates of benthonic primary production.This hypothesis suggests that the temporal correlation of major shifts in tectonic mode and at mospheric composition may not be fortuitous. It also suggests that sedimentary environments may have constituted a significant limit to the abundance and diversity of early life.Nothing is harder, yet nothing is more necessary, than to speak of certain things whose existence is neither demonstrable nor probable.Paper presented at the College Park Colloquia on Chemical Evolution, Limits of Life, University of Maryland, College Park, MD, October 18–20, 1978.     

A sluggish mid‐Proterozoic biosphere and its effect on Earth's redox balance

The possibility of low but nontrivial atmospheric oxygen (O₂) levels during the mid‐Proterozoic (between 1.8 and 0.8 billion years ago, Ga) has important ramifications for understanding Earth's O₂ cycle, the evolution of complex life and evolving climate stability. However, the regulatory mechanisms and redox fluxes required to stabilize these O₂ levels in the face of continued biological oxygen production remain uncertain. Here, we develop a biogeochemical model of the C‐N‐P‐O₂‐S cycles and use it to constrain global redox balance in the mid‐Proterozoic ocean–atmosphere system. By employing a Monte Carlo approach bounded by observations from the geologic record, we infer that the rate of net biospheric O₂ production was Tmol year^?1 (1σ), or ~25% of today's value, owing largely to phosphorus scarcity in the ocean interior. Pyrite burial in marine sediments would have represented a comparable or more significant O₂ source than organic carbon burial, implying a potentially important role for Earth's sulphur cycle in balancing the oxygen cycle and regulating atmospheric O₂ levels. Our statistical approach provides a uniquely comprehensive view of Earth system biogeochemistry and global O₂ cycling during mid‐Proterozoic time and implicates severe P biolimitation as the backdrop for Precambrian geochemical and biological evolution.     

Biogeochemical transformations after the emergence of oxygenic photosynthesis and conditions for the first rise of atmospheric oxygen

The advent of oxygenic photosynthesis represents the most prominent biological innovation in the evolutionary history of the Earth. The exact timing of the evolution of oxygenic photoautotrophic bacteria remains elusive, yet these bacteria profoundly altered the redox state of the ocean–atmosphere–biosphere system, ultimately causing the first major rise in atmospheric oxygen (O₂)—the so-called Great Oxidation Event (GOE)—during the Paleoproterozoic (~2.5–2.2 Ga). However, it remains unclear how the coupled atmosphere–marine biosphere system behaved after the emergence of oxygenic photoautotrophs (OP), affected global biogeochemical cycles, and led to the GOE. Here, we employ a coupled atmospheric photochemistry and marine microbial ecosystem model to comprehensively explore the intimate links between the atmosphere and marine biosphere driven by the expansion of OP, and the biogeochemical conditions of the GOE. When the primary productivity of OP sufficiently increases in the ocean, OP suppresses the activity of the anaerobic microbial ecosystem by reducing the availability of electron donors (H₂ and CO) in the biosphere and causes climate cooling by reducing the level of atmospheric methane (CH₄). This can be attributed to the supply of OH radicals from biogenic O₂, which is a primary sink of biogenic CH₄ and electron donors in the atmosphere. Our typical result also demonstrates that the GOE is triggered when the net primary production of OP exceeds >~5% of the present oceanic value. A globally frozen snowball Earth event could be triggered if the atmospheric CO₂ level was sufficiently small (<~40 present atmospheric level; PAL) because the concentration of CH₄ in the atmosphere would decrease faster than the climate mitigation by the carbonate–silicate geochemical cycle. These results support a prolonged anoxic atmosphere after the emergence of OP during the Archean and the occurrence of the GOE and snowball Earth event during the Paleoproterozoic.     

The evolving redox chemistry and bioavailability of vanadium in deep time

The incorporation of metal cofactors into protein active sites and/or active regions expanded the network of microbial metabolism during the Archean eon. The bioavailability of crucial metal cofactors is largely influenced by earth surface redox state, which impacted the timing of metabolic evolution. Vanadium (V) is a unique element in geo–bio‐coevolution due to its complex redox chemistry and specific biological functions. Thus, the extent of microbial V utilization potentially represents an important link between the geo‐ and biospheres in deep time. In this study, we used geochemical modeling and network analysis to investigate the availability and chemical speciation of V in the environment, and the emergence and changing chemistry of V‐containing minerals throughout earth history. The redox state of V shifted from a more reduced V(III) state in Archean aqueous geochemistry and mineralogy to more oxidized V(IV) and V(V) states in the Proterozoic and Phanerozoic. The weathering of vanadium sulfides, vanadium alkali metal minerals, and vanadium alkaline earth metal minerals were potential sources of V to the environment and microbial utilization. Community detection analysis of the expanding V mineral network indicates tectonic and redox influence on the distribution of V mineral‐forming elements. In reducing environments, energetic drivers existed for V to potentially be involved in early nitrogen fixation, while in oxidizing environments vanadate () could have acted as a metabolic electron acceptor and phosphate mimicking enzyme inhibitor. The coevolving chemical speciation and biological functions of V due to earth's changing surface redox conditions demonstrate the crucial links between the geosphere and biosphere in the evolution of metabolic electron transfer pathways and biogeochemical cycles from the Archean to Phanerozoic.     

Radiation of nitrogen‐metabolizing enzymes across the tree of life tracks environmental transitions in Earth history

Nitrogen is an essential element to life and exerts a strong control on global biological productivity. The rise and spread of nitrogen‐utilizing microbial metabolisms profoundly shaped the biosphere on the early Earth. Here, we reconciled gene and species trees to identify birth and horizontal gene transfer events for key nitrogen‐cycling genes, dated with a time‐calibrated tree of life, in order to examine the timing of the proliferation of these metabolisms across the tree of life. Our results provide new insights into the evolution of the early nitrogen cycle that expand on geochemical reconstructions. We observed widespread horizontal gene transfer of molybdenum‐based nitrogenase back to the Archean, minor horizontal transfer of genes for nitrate reduction in the Archean, and an increase in the proliferation of genes metabolizing nitrite around the time of the Mesoproterozoic (~1.5 Ga). The latter coincides with recent geochemical evidence for a mid‐Proterozoic rise in oxygen levels. Geochemical evidence of biological nitrate utilization in the Archean and early Proterozoic may reflect at least some contribution of dissimilatory nitrate reduction to ammonium (DNRA) rather than pure denitrification to N₂. Our results thus help unravel the relative dominance of two metabolic pathways that are not distinguishable with current geochemical tools. Overall, our findings thus provide novel constraints for understanding the evolution of the nitrogen cycle over time and provide insights into the bioavailability of various nitrogen sources in the early Earth with possible implications for the emergence of eukaryotic life.     

Cryoconite pans on Snowball Earth: supraglacial oases for Cryogenian eukaryotes?

Geochemical, paleomagnetic, and geochronological data increasingly support the Snowball Earth hypothesis for Cryogenian glaciations. Yet, the fossil record reveals no clear‐cut evolutionary bottleneck. Climate models and the modern cryobiosphere offer insights on this paradox. Recent modeling implies that Snowball continents never lacked ice‐free areas. Wind‐blown dust from these areas plus volcanic ash were trapped by snow on ice sheets and sea ice. At a Snowball onset, sea ice was too thin to flow and ablative ice was too cold for dust retention. After a few millenia, sea ice reached 100 s of meters in thickness and began to flow as a ‘sea glacier’ toward an equatorial ablation zone. At first, dust advected to the ablative surface was recycled by winds, but as the surface warmed with rising CO₂, dust aka cryoconite began to accumulate. As a sea glacier has no terminus, cryoconite saturated the surface. It absorbed solar radiation, supported cyanobacterial growth, and sank to an equilibrium depth forming holes and decameter‐scale pans of meltwater. As meltwater production rose, drainages developed, connecting pans to moulins, where meltwater was flushed into the subglacial ocean. Flushing cleansed the surface, creating a stabilizing feedback. If the dust flux rose, cryoconite was removed; if the dust flux waned, cryoconite accumulated. In addition to cyanobacteria, modern cryoconite holes are inhabited by green algae, fungi, protists, and certain metazoans. On Snowball Earth, cryoconite pans provided stable interconnected habitats for eukaryotes tolerant of fresh to brackish cold water on an ablation surface 60 million km² in area. Flushing and burial of organic matter was a potential source of atmospheric oxygen. Dominance of green algae among Ediacaran eukaryotic primary producers is a possible legacy of Cryogenian cryoconite pans, but a schizohaline ocean—supraglacial freshwater and subglacial brine—may have exerted selective stress on early metazoans, or impeded their evolution.     

Mass-independent fractionation of sulfur isotopes in sulfides from the pre-3770 Ma Isua Supracrustal Belt, West Greenland

Redox chemistry of the coupled atmosphere–hydrosphere system has coevolved with the biosphere, from global anoxia in the Archean to an oxygenated Proterozoic surface environment. However, to trace these changes to the very beginning of the rock record presents special challenges. All known Eoarchean (c. 3850–3600 Ma) volcanosedimentary successions (i.e. supracrustal rocks) are restricted to high‐grade gneissic terranes that seldom preserve original sedimentary structures and lack primary organic biomarkers. Although complicated by metamorphic overprinting, sulfur isotopes from Archean supracrustal rocks have the potential to preserve signatures of both atmospheric chemistry and metabolic fractionation from the original sediments. We present a synthesis of multiple sulfur isotope measurements (³²S, ³³S and ³⁴S) performed on sulfides from amphibolite facies banded iron‐formations (BIFs) and ferruginous garnet‐biotite (metapelitic) schists from the pre‐3770 Ma Isua Supracrustal Belt (ISB) in West Greenland. Because these data come from some of the oldest rocks of interpretable marine sedimentary origin, they provide the opportunity to (i) explore for possible biosignatures of sulfur metabolisms in early life; (ii) assess changes in atmospheric redox chemistry from ～3.8 Ga; and (iii) lay the groundwork to elucidate sulfur biogeochemical cycles on the early Earth. We find that sulfur isotope results from Isua do not unambiguously indicate microbially induced sulfur isotopic fractionation at that time. A significantly expanded data set of Δ³³S analyses for Isua dictates that the atmosphere was devoid of free oxygen at time of deposition and also shows that the effects of post‐depositional metamorphic remobilization and/or dilution can be traced in mass‐independently fractionated sulfur isotopes.     

Oceanic stable isotope composition and a scenario for the Permo‐Triassic crisis

Stable carbon isotope data from brachiopod shells from the Upper Permian Kapp Starostin Formation (West Spitsbergen) indicate that the oceanic carbon isotopic ratio, which had already been very high in the late Permian, rapidly increased by almost 4 per mil and then dramatically declined by more than 10 per mil in the very latest Permian. This pattern is essentially repeated by the oxygen isotope curve. These data show that a geologically rapid switch between two fundamentally different states of the Earth's exosystem occurred near the Permo‐Triassic transition. The late Permian state of the global system was profoundly different from the modern one in that vast amounts of organic carbon were stored, presumably in the form of easy‐to‐mobilize sapropel‐like deposits, below the oceanic redoxcline. Under such conditions—which we propose to call overfed ocean—nutrients were intensely recycled to seawater, thus allowing the ocean to sustain a huge standing crop of the biosphere. Deposition of large amounts of organic carbon in the ocean liberated corresponding amounts of oxygen, thus leading to high oxygen levels in the atmosphere. In the latest Permian, the organic matter decaying in the ocean was subject to rapid oxidation due to appearance of the modern type of ocean which is characterized by vigorous bottom circulation and net heterotrophy. The appearance of these conditions—which we propose to call hungry ocean—led to removal of nutrients from seawater and to a substantial drop in atmospheric oxygen contents. The resulting nutrient deficiency in the ocean, oxygen depletion in the atmosphere, and other effects of this paleoceanographic change must have caused major extinctions.     

Variations in the Properties of Extractable “Humic Matter” and Associated Kerogen in Sediments through Geologic Time: Their Significance for Precambrian Biological Evolution and Paleoecology

Chemical properties and δ¹³C values of benzene/methanol-extractable “humic matter” and associated kerogen in a large, diverse collection of Precambrian and Phanerozoic sediments from different parts of the world showed complex systematic variations through geologic time, reflecting major developments in the history of Precambrian life, and different kinds of sediment yielded similar patterns of variation. Moreover, certain data differentiate clearly between glacial and nonglacial detrital sediments, or between lacustrine and marine sediments, and some data suggest the occurrence of Precambrian land life. The abundance of aromatic groups and the proportion of aliphatic to aromatic groups in the extracts showed little variation from the early Archean (ca. 3.3 Ga) to the mid-Proterozoic (ca. 1.6-1.3 or 1.3-1.1 Ga), whereupon they increased sharply, peaked ca. 1.1-0.900 Ga, and then plunged to a minimum in the late Proterozoic (ca. 0.800 Ga) or early Phanerozoic. This is interpreted as indicating that cyanobacteria were the dominant photoautotrophs until the mid-Proterozoic, when algae evolved, proliferating until the late Proterozoic, whereupon their populations were depleted by herbivorous metazoans. Nitrogenous aromatic material increased to a maximum ca. 3.4–3.3 Ga and then decreased steadily to ca. 1.3 Ga, suggesting that early Precambrian cyanobacteria were enriched in photoprotective as well as photosynthetic tetrapyrrole pigments owing to the lack of ultraviolet radiation-shielding atmospheric O₂ and O₃. The concentration increased again starting ca. 1.3–0.800 Ga, reflecting the rise of algae, peaked ca. 0.680 Ga, and dropped catastrophically to a much lower value in the Cambrian (ca. 0.510 Ga), suggesting mass mortality at the Precambrian-Cambrian boundary.     

Modeling the carbon cycle in Lake Matano

Lake Matano, Indonesia, is a stratified anoxic lake with iron‐rich waters that has been used as an analogue for the Archean and early Proterozoic oceans. Past studies of Lake Matano report large amounts of methane production, with as much as 80% of primary production degraded via methanogenesis. Low δ¹³C values of DIC in the lake are difficult to reconcile with this notion, as fractionation during methanogenesis produces isotopically heavy CO₂. To help reconcile these observations, we develop a box model of the carbon cycle in ferruginous Lake Matano, Indonesia, that satisfies the constraints of CH₄ and DIC isotopic profiles, sediment composition, and alkalinity. We estimate methane fluxes smaller than originally proposed, with about 9% of organic carbon export to the deep waters degraded via methanogenesis. In addition, despite the abundance of Fe within the waters, anoxic ferric iron respiration of organic matter degrades <3% of organic carbon export, leaving methanogenesis as the largest contributor to anaerobic organic matter remineralization, while indicating a relatively minor role for iron as an electron acceptor. As the majority of carbon exported is buried in the sediments, we suggest that the role of methane in the Archean and early Proterozoic oceans is less significant than presumed in other studies.     

Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise in atmospheric oxygen

When cyanobacteria originated and diversified, and what their ancient traits were, remain critical unresolved problems. Here, we used a phylogenomic approach to construct a well‐resolved ‘core’ cyanobacterial tree. The branching positions of four lineages (Thermosynechococcus elongatus, Synechococcus elongatus, Synechococcus PCC 7335 and Acaryochloris marina) were problematic, probably due to long branch attraction artifacts. A consensus genomic tree was used to study trait evolution using ancestral state reconstruction (ASR). The early cyanobacteria were probably unicellular, freshwater, had small cell diameters, and lacked the traits to form thick microbial mats. Relaxed molecular clock analyses suggested that early cyanobacterial lineages were restricted to freshwater ecosystems until at least 2.4 Ga, before diversifying into coastal brackish and marine environments. The resultant increases in niche space and nutrient availability, and consequent sedimentation of organic carbon into the deep oceans, would have generated large pulses of oxygen into the biosphere, possibly explaining why oxygen rose so rapidly. Rapid atmospheric oxidation could have destroyed the methane‐driven greenhouse with simultaneous drawdown in pCO₂, precipitating ‘Snowball Earth’ conditions. The traits associated with the formation of thick, laminated microbial mats (large cell diameters, filamentous growth, sheaths, motility and nitrogen fixation) were not seen until after diversification of the LPP, SPM and PNT clades, after 2.32 Ga. The appearance of these traits overlaps with a global carbon isotopic excursion between 2.2 and 2.1 Ga. Thus, a massive re‐ordering of biogeochemical cycles caused by the appearance of complex laminated microbial communities in marine environments may have caused this excursion. Finally, we show that ASR may provide an explanation for why cyanobacterial microfossils have not been observed until after 2.0 Ga, and make suggestions for how future paleobiological searches for early cyanobacteria might proceed. In summary, key evolutionary events in the microbial world may have triggered some of the key geologic upheavals on the Paleoproterozoic Earth.     

A sedimentary record of the evolution of the global marine phosphorus cycle

Phosphorus (P) is typically considered to be the ultimate limiting nutrient for Earth's biosphere on geologic timescales. As P is monoisotopic, its sedimentary enrichment can provide some insights into how the marine P cycle has changed through time. A previous compilation of shale P enrichments argued for a significant change in P cycling during the Ediacaran Period (635–541 Ma). Here, using an updated P compilation—with more than twice the number of samples—we bolster the case that there was a significant transition in P cycling moving from the Precambrian into the Phanerozoic. However, our analysis suggests this state change may have occurred earlier than previously suggested. Specifically in the updated database, there is evidence for a transition ~35 million years before the onset of the Sturtian Snowball Earth glaciation in the Visingsö Group, potentially divorcing the climatic upheavals of the Neoproterozoic from changes in the Earth's P cycle. We attribute the transition in Earth's sedimentary P record to the onset of a more modern-like Earth system state characterized by less reducing marine conditions, higher marine P concentrations, and a greater predominance of eukaryotic organisms encompassing both primary producers and consumers. This view is consistent with organic biomarker evidence for a significant eukaryotic contribution to the preserved sedimentary organic matter in this succession and other contemporaneous Tonian marine sedimentary rocks. However, we stress that, even with an expanded dataset, we are likely far from pinpointing exactly when this transition occurred or whether Earth's history is characterized by a single or multiple transitions in the P cycle.