Christopher T. Reinhard

The rise of oxygen in Earth/'s early ocean and atmosphere

The rapid increase of carbon dioxide concentration in Earth’s modern atmosphere is a matter of major concern. But for the atmosphere of roughly two-and-half billion years ago, interest centres on a different gas: free oxygen (O2) spawned by early biological production. The initial increase of O2 in the atmosphere, its delayed build-up in the ocean, its increase to near-modern levels in the sea and air two billion years later, and its cause-and-effect relationship with life are among the most compelling stories in Earth’s history.

Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals

Low oxygen limited the rise of animals Oxygen levels in Earths early atmosphere had an important influence on the evolution of complex life. Planavsky et al. analyzed the isotopic signature of chromium in sedimentary rocks from across the globe—a proxy for past oxygen levels. Oxygen levels in the mid-Proterozoic (1.6 billion to 900 million years ago) were very low: less than 0.1% of the modern atmosphere. These low levels were probably below the minimum oxygen requirements for the earliest animals, delaying their emergence and diversification. Science, this issue p. 635 Oxygen levels in Earth’s early atmosphere were often less than 1% of modern levels. The oxygenation of Earth’s surface fundamentally altered global biogeochemical cycles and ultimately paved the way for the rise of metazoans at the end of the Proterozoic. However, current estimates for atmospheric oxygen (O2) levels during the billion years leading up to this time vary widely. On the basis of chromium (Cr) isotope data from a suite of Proterozoic sediments from China, Australia, and North America, interpreted in the context of data from similar depositional environments from Phanerozoic time, we find evidence for inhibited oxidation of Cr at Earth’s surface in the mid-Proterozoic (1.8 to 0.8 billion years ago). These data suggest that atmospheric O2 levels were at most 0.1% of present atmospheric levels. Direct evidence for such low O2 concentrations in the Proterozoic helps explain the late emergence and diversification of metazoans.

Widespread iron-rich conditions in the mid-Proterozoic ocean.

The chemical composition of the ocean changed markedly with the oxidation of the Earth’s surface, and this process has profoundly influenced the evolutionary and ecological history of life. The early Earth was characterized by a reducing ocean–atmosphere system, whereas the Phanerozoic eon (less than 542 million years ago) is known for a stable and oxygenated biosphere conducive to the radiation of animals. The redox characteristics of surface environments during Earth’s middle age (1.8–1 billion years ago) are less well known, but it is generally assumed that the mid-Proterozoic was home to a globally sulphidic (euxinic) deep ocean. Here we present iron data from a suite of mid-Proterozoic marine mudstones. Contrary to the popular model, our results indicate that ferruginous (anoxic and Fe2+-rich) conditions were both spatially and temporally extensive across diverse palaeogeographic settings in the mid-Proterozoic ocean, inviting new models for the temporal distribution of iron formations and the availability of bioessential trace elements during a critical window for eukaryotic evolution.

Proterozoic ocean redox and biogeochemical stasis

The partial pressure of oxygen in Earth’s atmosphere has increased dramatically through time, and this increase is thought to have occurred in two rapid steps at both ends of the Proterozoic Eon (∼2.5–0.543 Ga). However, the trajectory and mechanisms of Earth’s oxygenation are still poorly constrained, and little is known regarding attendant changes in ocean ventilation and seafloor redox. We have a particularly poor understanding of ocean chemistry during the mid-Proterozoic (∼1.8–0.8 Ga). Given the coupling between redox-sensitive trace element cycles and planktonic productivity, various models for mid-Proterozoic ocean chemistry imply different effects on the biogeochemical cycling of major and trace nutrients, with potential ecological constraints on emerging eukaryotic life. Here, we exploit the differing redox behavior of molybdenum and chromium to provide constraints on seafloor redox evolution by coupling a large database of sedimentary metal enrichments to a mass balance model that includes spatially variant metal burial rates. We find that the metal enrichment record implies a Proterozoic deep ocean characterized by pervasive anoxia relative to the Phanerozoic (at least ∼30–40% of modern seafloor area) but a relatively small extent of euxinic (anoxic and sulfidic) seafloor (less than ∼1–10% of modern seafloor area). Our model suggests that the oceanic Mo reservoir is extremely sensitive to perturbations in the extent of sulfidic seafloor and that the record of Mo and chromium enrichments through time is consistent with the possibility of a Mo–N colimited marine biosphere during many periods of Earth’s history.

The evolution of the marine phosphate reservoir

Phosphorus is a biolimiting nutrient that has an important role in regulating the burial of organic matter and the redox state of the ocean–atmosphere system. The ratio of phosphorus to iron in iron-oxide-rich sedimentary rocks can be used to track dissolved phosphate concentrations if the dissolved silica concentration of sea water is estimated. Here we present iron and phosphorus concentration ratios from distal hydrothermal sediments and iron formations through time to study the evolution of the marine phosphate reservoir. The data suggest that phosphate concentrations have been relatively constant over the Phanerozoic eon, the past 542 million years (Myr) of Earth’s history. In contrast, phosphate concentrations seem to have been elevated in Precambrian oceans. Specifically, there is a peak in phosphorus-to-iron ratios in Neoproterozoic iron formations dating from ∼750 to ∼635 Myr ago, indicating unusually high dissolved phosphate concentrations in the aftermath of widespread, low-latitude ‘snowball Earth’ glaciations. An enhanced postglacial phosphate flux would have caused high rates of primary productivity and organic carbon burial and a transition to more oxidizing conditions in the ocean and atmosphere. The snowball Earth glaciations and Neoproterozoic oxidation are both suggested as triggers for the evolution and radiation of metazoans. We propose that these two factors are intimately linked; a glacially induced nutrient surplus could have led to an increase in atmospheric oxygen, paving the way for the rise of metazoan life.

A late archean sulfidic sea stimulated by early oxidative weathering of the continents

Of Ancient Iron and Oxygen Finding clues to understand the early evolution of ocean and atmospheric chemistry and its links to the evolution of life remains a daunting task. Often just a few rock samples provide our only evidence of what conditions on Earth were like long ago. Reinhard et al. (p. 713) combined iron speciation data from a 2.5-billion-year-old shale from Australia with sulfur isotope data from this and nearby formations to conclude that oxygen chemistry predominanty consisted of an anoxic sulfide–rich water column, instead of iron-rich oceans, as previously speculated. Thus, brief pulses of reduced iron from hydrothermal vents may have been responsible for the formation of nearby banded iron formations and may have provided enough buffering to prolong the appearance of atmospheric oxygen generated by the expansion of newly evolved cyanobacteria. Before Earth’s atmosphere became oxidizing, the oceans may have been sulfide-rich while receiving periodic pulses of iron. Iron speciation data for the late Archean Mount McRae Shale provide evidence for a euxinic (anoxic and sulfidic) water column 2.5 billion years ago. Sulfur isotope data compiled from the same stratigraphic section suggest that euxinic conditions were stimulated by an increase in oceanic sulfate concentrations resulting from weathering of continental sulfide minerals exposed to an atmosphere with trace amounts of photosynthetically produced oxygen. Variability in local organic matter flux likely confined euxinic conditions to midportions of the water column on the basin margin. These findings indicate that euxinic conditions may have been common on a variety of spatial and temporal scales both before and immediately after the Paleoproterozoic rise in atmospheric oxygen, hinting at previously unexplored texture and variability in deep ocean chemistry during Earth’s early history.

Evolution of the global phosphorus cycle

The macronutrient phosphorus is thought to limit primary productivity in the oceans on geological timescales. Although there has been a sustained effort to reconstruct the dynamics of the phosphorus cycle over the past 3.5 billion years, it remains uncertain whether phosphorus limitation persisted throughout Earth’s history and therefore whether the phosphorus cycle has consistently modulated biospheric productivity and ocean–atmosphere oxygen levels over time. Here we present a compilation of phosphorus abundances in marine sedimentary rocks spanning the past 3.5 billion years. We find evidence for relatively low authigenic phosphorus burial in shallow marine environments until about 800 to 700 million years ago. Our interpretation of the database leads us to propose that limited marginal phosphorus burial before that time was linked to phosphorus biolimitation, resulting in elemental stoichiometries in primary producers that diverged strongly from the Redfield ratio (the atomic ratio of carbon, nitrogen and phosphorus found in phytoplankton). We place our phosphorus record in a quantitative biogeochemical model framework and find that a combination of enhanced phosphorus scavenging in anoxic, iron-rich oceans and a nutrient-based bistability in atmospheric oxygen levels could have resulted in a stable low-oxygen world. The combination of these factors may explain the protracted oxygenation of Earth’s surface over the last 3.5 billion years of Earth history. However, our analysis also suggests that a fundamental shift in the phosphorus cycle may have occurred during the late Proterozoic eon (between 800 and 635 million years ago), coincident with a previously inferred shift in marine redox states, severe perturbations to Earth’s climate system, and the emergence of animals.

Late Archean euxinic conditions before the rise of atmospheric oxygen

Life on Earth is thought to have coevolved with the chemistry of the oceans and atmosphere, and the shift from an anoxic to an oxic world across the Archean-Proterozoic boundary represents a fundamental step in this process. In order to understand the relative influence of biological and geological factors on this transition, we must constrain key variables in seawater chemistry before the Great Oxidation Event (ca. 2500 Ma). We present a multielement (C-S-Fe-Mo) biogeochemical study of ca. 2662 Ma shales from the Hamersley Province in Western Australia. Our data reveal a sustained episode of Fe-limited pyrite formation under an anoxic and sulfidic (euxinic) water column. This is the oldest known occurrence of euxinia in Earth9s history and challenges the paradigm of persistently Fe-rich Archean oceans. Bulk trace metal chemistry and preservation of strong mass-independent S isotope fractionations in sedimentary pyrites indicate that ocean euxinia was possible prior to oxidative weathering, suggesting that sulfidic waters may have been common throughout the Archean Eon. C-S-Fe systematics suggest that oxygenic photosynthesis was the primary source of organic carbon in the basin, and the absence of Mo enrichments highlights a potential link between inefficient nitrogen fixation and the delayed arrival of the Great Oxidation Event.

A shale-hosted Cr isotope record of low atmospheric oxygen during the Proterozoic

The emergence and expansion of animal life on Earth represents a dramatic shift in the structure and complexity of the biosphere. A lack of firm constraints on surface oxygen levels during the mid-Proterozoic has resulted in heated debate as to whether the rise and earliest diversification of animals was directly linked to a change in environmental oxygen levels or, instead, simply reflects the timing of innovations in gene expression and developmental regulation and was independent of a direct environmental trigger. Here, we present chromium (Cr) isotope data from marine black shales that provide evidence for minimal Cr oxidation throughout the mid-Proterozoic leading up to the diversification of eukaryotes and the rise of animals during the late Neoproterozoic. This observation requires very low background oxygen levels (<1% of present atmospheric levels). Accepting previously proposed estimates of p O2 levels needed to induce Cr isotope fractionation, our data provide support for the persistence of an Earth system in which baseline atmospheric p O2 would have been low enough to inhibit the diversification of animals until ca. 800 Ma. More generally, evidence for a delayed rise of atmospheric oxygen strongly suggests that environmental factors have played a fundamental role in controlling the emergence and expansion of complex life on Earth.

Earth’s oxygen cycle and the evolution of animal life

Significance Earth is currently the only planet known to harbor complex life. Understanding whether terrestrial biotic complexity is a unique phenomenon or can be expected to be widespread in the universe depends on a mechanistic understanding of the factors that led to the emergence of complex life on Earth. Here, we use geochemical constraints and quantitative models to suggest that marine environments may have been unfavorable for the emergence and large-scale proliferation of motile multicellular life for most of Earth’s history. Further, we argue that a holistic evaluation of environmental variability, organismal life history, and spatial ecological dynamics is essential for a full accounting of the factors that have allowed for the emergence of biological complexity on Earth. The emergence and expansion of complex eukaryotic life on Earth is linked at a basic level to the secular evolution of surface oxygen levels. However, the role that planetary redox evolution has played in controlling the timing of metazoan (animal) emergence and diversification, if any, has been intensely debated. Discussion has gravitated toward threshold levels of environmental free oxygen (O2) necessary for early evolving animals to survive under controlled conditions. However, defining such thresholds in practice is not straightforward, and environmental O2 levels can potentially constrain animal life in ways distinct from threshold O2 tolerance. Herein, we quantitatively explore one aspect of the evolutionary coupling between animal life and Earth’s oxygen cycle—the influence of spatial and temporal variability in surface ocean O2 levels on the ecology of early metazoan organisms. Through the application of a series of quantitative biogeochemical models, we find that large spatiotemporal variations in surface ocean O2 levels and pervasive benthic anoxia are expected in a world with much lower atmospheric pO2 than at present, resulting in severe ecological constraints and a challenging evolutionary landscape for early metazoan life. We argue that these effects, when considered in the light of synergistic interactions with other environmental parameters and variable O2 demand throughout an organism’s life history, would have resulted in long-term evolutionary and ecological inhibition of animal life on Earth for much of Middle Proterozoic time (∼1.8–0.8 billion years ago).