Earth's oxygen revolution

Brian Kendall, Department of Earth and Environmental Sciences, University of Waterloo

Figure 1. Earth's surface oxygenation through time and its relationship to significant steps in biological evolution. The upper panel shows atmospheric oxygen abundances in % relative to present atmospheric levels (PAL). The lower panel shows the relative distribution of oxygen- (O₂), sulfide- (H₂S), and iron-rich (Fe²⁺) waters in the shallow and deep oceans. Lighter blue shading indicates lower dissolved O₂ levels. Lighter pink shading means less H₂S and more Fe²⁺.

What triggered atmospheric oxygenation? The evolution of oxygenic photosynthesis was undoubtedly a pre-requisite because this is the single most important source of O₂ to Earth's surface. However, it was probably not the only factor. There is growing evidence for photosynthetic O₂ production and accumulation in surface waters along some coastal regions ("oxygen oases") at least a few hundred million years before the Great Oxidation Event. These oxygen oases may have even hosted the first O_2-respiring eukaryotes.

Why then did the Great Oxidation Event take so long to occur? Oxygen had to first overwhelm the flux of reductants (e.g., H₂, CH₄) before it could accumulate in the atmosphere. Photosynthetic O₂ accumulation in the surface oceans may have started off slowly. A progressive loss of hydrogen to space or a decreased flux of reducing volcanic gases may have been needed to tip the scales towards oxygenation. Multiple severe glaciations (extending to tropical latitudes) may have played a role. High atmospheric CO₂ levels are needed to end a severe glaciation. The resulting hot climate would have promoted intense weathering-related release of nutrients (furthered by glacial erosion) and thus high rates of primary productivity on tropical continental shelves. Large amounts of organic matter (dead primary producers) are then buried in sediments. Buried organic matter cannot react with O₂, which accumulates in the atmosphere (Figure 2).

Figure 2. Relationship between photosynthesis, organic matter burial, and oxygenation. An increase in nutrients to the oceans will stimulate primary productivity, including photosynthesis. Decay of sinking organic matter will consume dissolved oxygen, a process that is contributing to deoxygenation of the coastal oceans today. On longer (geologic) time scales, however, high rates of nutrient delivery to the oceans can cause burial of large amounts of organic matter (CH₂O). Oxygen produced by photosynthesis cannot react with the buried organic matter and thus the gas accumulates on the Earth's surface.

Figure 3. Glacial sediments deposited ~670 million years ago in an ocean basin. This type of rock is called diamictite, and consists of a poorly sorted mixture of large and small clasts surrounded by a finer-grained sediment matrix. Note the coin for scale. Areyonga Formation, Amadeus Basin, central Australia. Photo credit: R.A. Creaser.

For the first time in Earth's history, the oceans contained enough dissolved O₂ to support large complex animal life. Shortly after the end of the Snowball glaciation and the increase in ocean oxygenation, the first large complex animals appear in the rock record, including those that could move and prey on other organisms. A series of dizzyingly rapid evolutionary innovations driven by environmental, genetic, and ecological factors then culminated in a "Cambrian Explosion" (named for the Cambrian Period in which it occurs) of skeletal animal life some 540 to 520 Myr ago. It is remarkable that it took four billion years of Earth history for evolution to produce animal life, and that catastrophic glaciations played a role in doing so.

Conventional thinking is that the Earth's atmosphere and oceans have been well-oxygenated since then. However, recent findings suggest lower atmospheric O₂ levels and large oscillations in oceanic O₂ levels between 635 and 400 Myr ago. Another O₂ boost may have been triggered by the diversification of land plants 400 Myr ago. Land plants enable more efficient organic matter burial by accelerating the rate of continental weathering. Organic plant material can also be highly resistant to degradation and be buried more easily. The resulting increase in O₂ levels may have stimulated the evolution of large predatory fish. Diversification of land plants and formation of the supercontinent Pangaea likely played major roles in burying enough organic matter to generate the highest atmospheric O₂ levels in Earth's history 300-275 Myr ago.        

Although the Earth's oceans were predominantly oxygenated during the past 400 Myr, there were brief intervals called "ocean anoxic events" that were accompanied by a mass extinction of life. Ocean deoxygenation was typically caused by a warm climate (high atmospheric CO₂) and poor ocean circulation. During the anoxic event, higher rates of organic matter burial and continental weathering consumed the excess atmospheric CO₂. The drop in CO₂ promoted a return to colder oceans (favoring greater oxygen solubility and ocean circulation) and lower nutrient inventories for primary producers (less consumption of O₂ by decay of organic matter). Together with the preceding organic matter burial (O₂ release), these changes allowed the re-establishment of oxygenated oceans. The Earth's worst mass extinction was suffered during an ocean anoxic event 250 million years ago. Geoscientists scrutinize these events closely to better predict the future extent of ocean deoxygenation and its impact on human civilization.

Finally, how do geoscientists reconstruct the history of Earth's surface oxygenation? Our clues come from sediments deposited in Earth's ancient oceans, now preserved as layers of sedimentary rock. We can sample these rocks at the Earth's surface where they have been exposed by erosion (outcrops) or by human activities (mines, road cuts). Alternatively, we can obtain samples by drilling deep below the surface (Figure 4). Geoscientists prefer drill cores because the recovered rocks have not been affected by weathering reactions at Earth's surface.

Figure 4. Organic-rich black shale deposited ~2500 million years ago in deep ocean waters. Shale is composed of fine-grained sediment (<0.0625 mm particle size) and is fissile (split easily into thin paper-like sheets). Also visible are thin laminations and nodules of metallic brass-yellow pyrite ("fool's gold"). Mt. McRae Shale, Hamersley Basin, Western Australia. Photo credit: B. Kendall.

Our preferred method for reconstructing the story of atmosphere and ocean oxygenation is to study the distribution of oxygen-sensitive elements and minerals in sedimentary rocks. One example is the massive iron formations (the major source of industrial iron ore) deposited before the Great Oxidation Event and during the volcanic episode 1900 Myr ago (Figure 5). Their formation requires that large amounts of dissolved Fe2+ accumulate in predominantly oxygen- and sulfur-free oceans. Another example is the abundance of redox-sensitive metals like molybdenum (Mo) and vanadium (V) in organic-rich sediments (Figure 6). In the presence of O₂, these metals are weathered from the continents and transported by rivers to the oceans where they accumulate in oxygenated seawater. Upon encountering anoxic conditions, Mo and V are removed from seawater to sediments. Metal abundances in the sediments (now black shales) can be used to infer ancient seawater metal concentrations and the extent of oxygenation. High amounts of Mo and V in black shales indicate a large metal inventory in widely oxygenated oceans. By contrast, low amounts of Mo and V in black shales point to negligible oxidative weathering or O₂-deficient oceans (which favors high rates of metal burial in sediments).

Figure 5. Abundance of iron formations through time. Most iron formation was deposited early in Earth's history when the oceans were predominantly anoxic and Fe2+-rich. As a consequence of the Great Oxidation Event, the amount of dissolved Fe2+ in the oceans was significantly reduced by reaction with oxygen, sulfate, and sulfide, thus largely preventing further deposition of iron formation. An exception occurred about 1900 million years ago, when intense volcanism supplied large amounts of Fe2+ to the oceans. After this time, iron formation is scarce in the rock record. Modified from Rasmussen et al. (2012).

Figure 6. Abundance of molybdenum (Mo) and vanadium (V) in black shales through time. The abundances are reported as parts per million (p.p.m.), where 1 p.p.m. means 1 × 10^-6 gram of Mo (or V) per gram of shale. Metal concentrations are also divided (or "normalized") to total organic carbon content (TOC; given as weight % of the shale) to correct for variable amounts of organic matter in the sediment. It can be seen that Mo and V concentrations in black shales have increased through time, reflecting the growth of the oceanic inventory of these metals in response to ocean oxygenation. Major increases in metal concentration are observed in response to the Great Oxidation Event (2400-2100 million years ago) and shortly after a "Snowball Earth" glaciation 635 million years ago. Modified from Sahoo et al. (2012).