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.

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 pO 2 levels needed to induce Cr isotope fractionation, our data provide support for the persistence of an Earth system in which baseline atmospheric pO 2 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.

Few topics in geobiology have been as extensively debated as the role of Earth's oxygenation in controlling when and why animals emerged and diversified. All currently described animals require oxygen for at least a portion of their life cycle. Therefore, the transition to an oxygenated planet was a prerequisite for the emergence of animals. Yet, our understanding of Earth's oxygenation and the environmental requirements of animal habitability and ecological success is currently limited; estimates for the timing of the appearance of environments sufficiently oxygenated to support ecologically stable populations of animals span a wide range, from billions of years to only a few million years before animals appear in the fossil record. In this light, the extent to which oxygen played an important role in controlling when animals appeared remains a topic of debate. When animals originated and when they diversified are separate questions, meaning either one or both of these phenomena could have been decoupled from oxygenation. Here, we present views from across this interpretive spectrum—in a point–counterpoint format—regarding crucial aspects of the potential links between animals and surface oxygen levels. We highlight areas where the standard discourse on this topic requires a change of course and note that several traditional arguments in this “life versus environment” debate are poorly founded. We also identify a clear need for basic research across a range of fields to disentangle the relationships between oxygen availability and emergence and diversification of animal life.

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The oxygenation of the atmosphere — one of the most fundamental transformations in Earth's history — dramatically altered the chemical composition of the oceans and provides a compelling example of how life can reshape planetary surface environments. Furthermore, it is commonly proposed that surface oxygen levels played a key role in controlling the timing and tempo of the origin and early diversification of animals. Although oxygen levels were likely more dynamic than previously imagined, we make a case here that emerging records provide evidence for low atmospheric oxygen levels for the majority of Earth's history. Specifically, we review records and present a conceptual framework that suggest that background oxygen levels were below 1% of the present atmospheric level during the billon years leading up to the diversification of early animals. Evidence for low background oxygen levels through much of the Proterozoic bolsters the case that environmental conditions were a critical factor in controlling the structure of ecosystems through Earth's history.