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

Abstract

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.

Earth’s oxygen cycle and the evolution of animal life

“…This relationship may, in part, explain the early rise but protracted diversification of eukaryotes (34). More broadly, we stress that geochemical reconstructions of background atmospheric pO 2 (11,26) and experimental/theoretical reconstructions of resting O 2 demand in basal animal organisms (12,13), although critical, only provide part of the picture. Proterozoic marine environments would have been characterized by O 2 levels that departed strongly from background mean pO 2 , and the oxygen demand and marine habitat of different life history stages could present physiological bottlenecks that are currently poorly known for basal metazoan organisms.…”

“…Finally, we build on these perspectives to propose a simple conceptual model that frames the links between Earth's oxygen cycle and the early evolution of animal life as a question of habitat viability, highlighting the stability of environmental O 2 levels (e.g., ref. 25) against the backdrop of evolving baseline pO 2 (11,26), rather than the attainment of threshold O 2 levels for a single life history stage (10,11,23). We suggest that this view provides a more realistic and powerful framework for understanding the links between environmental stress and the early evolution of complex metazoan life on Earth.…”

Paleoproterozoic sterol biosynthesis and the rise of oxygen

“…Efforts to reconstruct environmental pO 2 through this interval (Cole et al, 2016;Lyons et al, 2014) will provide further sampling guidelines. The results of these endeavors will ultimately determine how well the fossil, geochemical, and molecular records for the rise of complex life might be reconciled with those for environmental oxygenation.…”

Animal origins and the Tonian Earth system

“…800-750 Ma [51,52] (Figure 3C) broadly correlated to the estimated age of the metazoan LCA, cited in these studies as ca. 800 Ma [53].…”

“…Indeed, the correlation between the estimated age of crown-group florideophytes taxa described per fossiliferous stratigraphic unit), taken from ref. [45]; (C) chromium isotope record aggregated from multiple studies [51,52,54,[77][78][79]; (D) Sterane/hopane ratios from ref. [55] and (E) relative fractions of cholestane, ergostane, and stigmastane (C27, C28, and C29, respectively) from ref.…”