Stabilization of the coupled oxygen and phosphorus cycles by the evolution of bioturbation

This is the author accepted manuscript. The final version is available from Nature Research via the DOI in this record Animal burrowing and sediment-mixing (bioturbation) began during the run up to the Ediacaran/Cambrian boundary, initiating a transition between the stratified Precambrian and more well-mixed Phanerozoic sedimentary records, against the backdrop of a variable global oxygen reservoir probably smaller in size than present. Phosphorus is the long-term limiting nutrient for oxygen production via burial of organic carbon, and its retention (relative to carbon) within organic matter in marine sediments is enhanced by bioturbation. Here we explore the biogeochemical implications of a bioturbation-induced organic phosphorus sink in a simple model. We show that increased bioturbation robustly triggers a net decrease in the size of the global oxygen reservoir - the magnitude of which is contingent upon the prescribed difference in carbon to phosphorus ratios between bioturbated and laminated sediments. Bioturbation also reduces steady-state marine phosphate levels, but this effect is offset by the decline in iron-adsorbed phosphate burial that results from a decrease in oxygen concentrations. The introduction of oxygen-sensitive bioturbation to dynamical model runs is sufficient to trigger a negative feedback loop: the intensity of bioturbation is limited by the oxygen decrease it initially causes. The onset of this feedback is consistent with redox variations observed during the early Cambrian rise of bioturbation, leading us to suggest that bioturbation helped to regulate early oxygen and phosphorus cycles. © 2014 Macmillan Publishers Limited. All rights reserved.Natural Environment Research Council (NERC)Inge Lehmann ScholarshipVILLUM FoundationNational Basic Research Program of ChinaNational Natural Science Foundation of ChinaDeutsche Forschungsgemeinschaft (DFG

A global transition to ferruginous conditions in the early Neoproterozoic oceans

Eukaryotic life expanded during the Proterozoic eon1, 2.5 to 0.542 billion years ago, against a background of fluctuating ocean chemistry2, 3, 4. After about 1.8 billion years ago, the global ocean is thought to have been characterized by oxygenated surface waters, with anoxic and sulphidic waters in middle depths along productive continental margins and anoxic and iron-containing (ferruginous) deeper waters5, 6, 7. The spatial extent of sulphidic waters probably varied through time5, 6, but this surface-to-deep redox structure is suggested to have persisted until the first Neoproterozoic glaciation about 717 million years ago8, 9, 10, 11. Here we report an analysis of ocean redox conditions throughout the Proterozoic using new and existing iron speciation and sulphur isotope data from multiple cores and outcrops. We find a global transition from sulphidic to ferruginous mid-depth waters in the earliest Neoproterozoic, coincident with the amalgamation of the supercontinent Rodinia at low latitudes. We suggest that ferruginous conditions were initiated by an increase in the oceanic influx of highly reactive iron relative to sulphate, driven by a change in weathering regime and the uptake of sulphate by extensive continental evaporites on Rodinia. We propose that this transition essentially detoxified ocean margin settings, allowing for expanded opportunities for eukaryote diversification following a prolonged evolutionary stasis before one billion years ago

Early Palaeozoic ocean anoxia and global warming driven by the evolution of shallow burrowing

The evolution of burrowing animals forms a defining event in the history of the Earth. It has been hypothesised that the expansion of seafloor burrowing during the Palaeozoic altered the biogeochemistry of the oceans and atmosphere. However, whilst potential impacts of bioturbation on the individual phosphorus, oxygen and sulphur cycles have been considered, combined effects have not been investigated, leading to major uncertainty over the timing and magnitude of the Earth system response to the evolution of bioturbation. Here we integrate the evolution of bioturbation into the COPSE model of global biogeochemical cycling, and compare quantitative model predictions to multiple geochemical proxies. Our results suggest that the advent of shallow burrowing in the early Cambrian contributed to a global low-oxygen state, which prevailed for ~100 million years. This impact of bioturbation on global biogeochemistry likely affected animal evolution through expanded ocean anoxia, high atmospheric CO2 levels and global warming

Selenium isotope evidence for progressive oxidation of the Neoproterozoic biosphere

Neoproterozoic (1,000–542 Myr ago) Earth experienced profound environmental change, including ‘snowball’ glaciations, oxygenation and the appearance of animals. However, an integrated understanding of these events remains elusive, partly because proxies that track subtle oceanic or atmospheric redox trends are lacking. Here we utilize selenium (Se) isotopes as a tracer of Earth redox conditions. We find temporal trends towards lower δ82/76Se values in shales before and after all Neoproterozoic glaciations, which we interpret as incomplete reduction of Se oxyanions. Trends suggest that deep-ocean Se oxyanion concentrations increased because of progressive atmospheric and deep-ocean oxidation. Immediately after the Marinoan glaciation, higher δ82/76Se values superpose the general decline. This may indicate less oxic conditions with lower availability of oxyanions or increased bioproductivity along continental margins that captured heavy seawater δ82/76Se into buried organics. Overall, increased ocean oxidation and atmospheric O2 extended over at least 100 million years, setting the stage for early animal evolution

Unique Neoproterozoic carbon isotope excursions sustained by coupled evaporite dissolution and pyrite burial

The Neoproterozoic era witnessed a succession of biological innovations that culminated in diverse animal body plans and behaviours during the Ediacaran–Cambrian radiations. Intriguingly, this interval is also marked by perturbations to the global carbon cycle, as evidenced by extreme fluctuations in climate and carbon isotopes. The Neoproterozoic isotope record has defied parsimonious explanation because sustained 12C-enrichment (low δ13C) in seawater seems to imply that substantially more oxygen was consumed by organic carbon oxidation than could possibly have been available. We propose a solution to this problem, in which carbon and oxygen cycles can maintain dynamic equilibrium during negative δ13C excursions when surplus oxidant is generated through bacterial reduction of sulfate that originates from evaporite weathering. Coupling of evaporite dissolution with pyrite burial drives a positive feedback loop whereby net oxidation of marine organic carbon can sustain greenhouse forcing of chemical weathering, nutrient input and ocean margin euxinia. Our proposed framework is particularly applicable to the late Ediacaran ‘Shuram’ isotope excursion that directly preceded the emergence of energetic metazoan metabolisms during the Ediacaran–Cambrian transition. Here we show that non-steady-state sulfate dynamics contributed to climate change, episodic ocean oxygenation and opportunistic radiations of aerobic life during the Neoproterozoic era

Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon

It is unclear why atmospheric oxygen remained trapped at low levels for more than 1.5 billion years following the Paleoproterozoic Great Oxidation Event. Here, we use models for erosion, weathering and biogeochemical cycling to show that this can be explained by the tectonic recycling of previously accumulated sedimentary organic carbon, combined with the oxygen sensitivity of oxidative weathering. Our results indicate a strong negative feedback regime when atmospheric oxygen concentration is of order pO2∼0.1 PAL (present atmospheric level), but that stability is lost at pO2<0.01 PAL. Within these limits, the carbonate carbon isotope (δ13C) record becomes insensitive to changes in organic carbon burial rate, due to counterbalancing changes in the weathering of isotopically light organic carbon. This can explain the lack of secular trend in the Precambrian δ13C record, and reopens the possibility that increased biological productivity and resultant organic carbon burial drove the Great Oxidation Event

A tectonically driven Ediacaran oxygenation event.

The diversification of complex animal life during the Cambrian Period (541-485.4 Ma) is thought to have been contingent on an oxygenation event sometime during ~850 to 541 Ma in the Neoproterozoic Era. Whilst abundant geochemical evidence indicates repeated intervals of ocean oxygenation during this time, the timing and magnitude of any changes in atmospheric pO₂ remain uncertain. Recent work indicates a large increase in the tectonic CO₂ degassing rate between the Neoproterozoic and Paleozoic Eras. We use a biogeochemical model to show that this increase in the total carbon and sulphur throughput of the Earth system increased the rate of organic carbon and pyrite sulphur burial and hence atmospheric pO₂. Modelled atmospheric pO₂ increases by ~50% during the Ediacaran Period (635-541 Ma), reaching ~0.25 of the present atmospheric level (PAL), broadly consistent with the estimated pO₂ > 0.1-0.25 PAL requirement of large, mobile and predatory animals during the Cambrian explosion

Anaerobic animals from an ancient, anoxic ecological niche

Tiny marine animals that complete their life cycle in the total absence of light and oxygen are reported by Roberto Danovaro and colleagues in this issue of BMC Biology. These fascinating animals are new members of the phylum Loricifera and possess mitochondria that in electron micrographs look very much like hydrogenosomes, the H2-producing mitochondria found among several unicellular eukaryotic lineages. The discovery of metazoan life in a permanently anoxic and sulphidic environment provides a glimpse of what a good part of Earth's past ecology might have been like in 'Canfield oceans', before the rise of deep marine oxygen levels and the appearance of the first large animals in the fossil record roughly 550-600 million years ago. The findings underscore the evolutionary significance of anaerobic deep sea environments and the anaerobic lifestyle among mitochondrion-bearing cells. They also testify that a fuller understanding of eukaryotic and metazoan evolution will come from the study of modern anoxic and hypoxic habitats