Earth’s oxygen cycle and the evolution of animal life

Abstract

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 (O 2 ) necessary for early evolving animals to survive under controlled conditions. However, defining such thresholds in practice is not straightforward, and environmental O 2 levels can potentially constrain animal life in ways distinct from threshold O 2 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 O 2 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 O 2 levels and pervasive benthic anoxia are expected in a world with much lower atmospheric pO 2 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 O 2 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).oxygen | animals | evolution | Proterozoic A long-standing and pervasive view is that there have been intimate mechanistic links between the evolution of complex life on Earth-in other words, the emergence and ecological expansion of eukaryotic cells and their aggregation into multicellular organisms-and the secular evolution of ocean−atmosphere oxygen levels (1). Molecular oxygen (O 2 ) is by far the most energetic of the abundant terminal oxidants used in biological metabolism (e.g., ref.2). When this energetic capacity is harnessed by mitochondria in eukaryotic cells, the energy flux supported by a given genome size increases by a factor of ∼8,000 (3), potentially paving the way for increased complexity at the cellular level (but see ref. 4). Oxygen is also a crucial component of enzymatic pathways leading to the synthesis of regulatory membrane lipids (5) and structural proteins (6) in eukaryotic organisms and provides a powerful shield against solar UV radiation at Earth's surface through stratospheric ozone production. Furthermore, O 2 is the only respiratory electron acceptor that can meet the metabolic demands required for attaining the large sizes and active lifestyles characteristic of metazoan life (e.g., ref. 7). There is thus ample support for the view that Earth's oxygen cycle provided a crucial evolutionary and ecological constraint on the road to increased biotic complexity, both at the cellular level and on the road ...

A model for the oceanic mass balance of rhenium and implications for the extent of Proterozoic ocean anoxia

“…This observation, independent of the model constraints, points to generally low O 2 concentrations in post-GOE oceans prior to stage records for Cr enrichment (Reinhard et al, 2013a) and isotopic trends Cole et al, 2016). However, as stressed by Partin et al (2013), Cole et al (2016), and Reinhard et al (2016), such an interpretation is only meant to represent the first-order marine redox landscape and does not preclude the possibility of spatiotemporal variations in atmosphere-ocean redox during midProterozoic time. Indeed, the higher average [Re] sed values from the ca.…”

“…Our interpretation is also consistent with Mo concentration and isotope data for these ORM (Kendall et al, 2009(Kendall et al, , 2015b, which constrain the extent of ocean euxinia rather than general ocean anoxia (euxinic plus ferruginous conditions). The model does not preclude the possibility that a significant portion of the low-productivity regions of the deep oceans may have been covered by weakly oxygenated waters (Slack et al, 2007(Slack et al, , 2009, nor does it preclude oxygenated surface waters in highly productive regions (Sperling et al, 2014;Reinhard et al, 2016).…”

“…Although low O 2 levels have been suggested for the midProterozoic atmosphere-ocean system (<0.1-1.0% PAL; Canfield, 1998;Reinhard et al, 2013a;Planavsky et al, 2014;Liu et al, 2016;Tang et al, 2016;Hardisty et al, 2017), such conditions imply poorly buffered surface O 2 inventories and the potential for significant spatiotemporal variability Cole et al, 2016;Reinhard et al, 2016;Daines et al, 2017;Hardisty et al, 2017). Indeed, there has been much recent interest in the possibility of dynamic spatiotemporal variations in atmosphere-ocean redox conditions during this time (e.g., Sperling et al, 2014;Gilleaudeau and Kah, 2015;Gilleaudeau et al, 2016;Mukherjee and Large, 2016;Planavsky et al, 2016;Reinhard et al, 2016;Zhang et al, 2016) against a background of lower atmospheric pO 2 compared with today (e.g., Cole et al, 2016).…”

“…Indeed, there has been much recent interest in the possibility of dynamic spatiotemporal variations in atmosphere-ocean redox conditions during this time (e.g., Sperling et al, 2014;Gilleaudeau and Kah, 2015;Gilleaudeau et al, 2016;Mukherjee and Large, 2016;Planavsky et al, 2016;Reinhard et al, 2016;Zhang et al, 2016) against a background of lower atmospheric pO 2 compared with today (e.g., Cole et al, 2016). Hence, additional data and proxies sensitive to global redox conditions are needed to better understand the spatiotemporal evolution and the dominant redox state of the mid-Proterozoic oceans.…”

Animal origins and the Tonian Earth system

“…Whether the billion-year macroevolutionary gap separating the LECA from the LCA of animals was primarily dictated by environmental-ecological conditions [6,46] or evolutionary contingency [33,40] remains debated (and perhaps an overly simplistic dichotomy -ref. [47]), although animal monophyly is arguably more consistent with the latter scenario [1,[31][32][33]. For example, it has been predicted that coloniality in the unicellular ancestors of animals was selected for its benefits in avoiding engulfment by predatory ciliates and other eukaryote-eating protists, which apparently evolved sometime in the Neoproterozoic Era [6,46].…”