Earth's oxygen revolution

Friday, March 1, 2013

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

Take a deep breath! This simple act provides your body with life-giving oxygen and removes waste carbon dioxide. It is part of what we call respiration, in which the chemical energy of organic molecules (derived from the food we eat) is released during a reaction that consumes oxygen and liberates water and carbon dioxide. During a single day, an adult will take about 20,000 breaths. Although essential for our survival, we routinely take each breath for granted as we proceed with our busy lives. Have you ever wondered when and why oxygen became so prevalent on Earth? Or how Earth surface's oxygenation is intertwined with the evolution of life?
Why do we care about the past distribution of oxygen on Earth's surface? Human activities, including fossil fuel burning and deforestation, are pumping greenhouse gases like carbon dioxide into the atmosphere. The Earth is getting warmer. What are the future consequences? We can expect a decline in ocean oxygen concentrations. Oxygen solubility in water decreases with increasing temperature. Continental weathering accelerates on a warmer Earth, delivering more nutrients (e.g., phosphorus) to the coastal oceans. Adding to this nutrient load is fertilizer runoff. These extra nutrients enhance the growth of primary producers and after these organisms die, the decay of their organic matter consumes oxygen. Declining ocean oxygen levels threaten to decimate the coastal marine biosphere, including fisheries - the main source of protein to many countries. Warm-season "dead zones", which contain too little O2 (< 2 mg/L) to support large fauna, are expanding. To understand and manage this threat, we are motivated to learn the lessons of the past by "reading the rock record" about the past history of ocean oxygenation.
On a more positive note, astronomers have discovered hundreds of planets outside our solar system. The search for Earth-sized planets in the "habitable zone" - the region around a star where liquid water might exist on a planet's surface - has commenced in earnest (e.g., NASA's Kepler mission). Such planets could potentially support complex life. How might the geological history and the course of biological evolution on other habitable planets be different from our own? Of course, the big motivator driving us is the search for intelligent life elsewhere in the universe. Oxygen is thought to be a pre-requisite for the evolution of complex animal and intelligent life. A logical step for us is to search for oxygen-rich worlds. To guide our efforts, we seek to understand the co-evolution of life and environment on Earth.
Today, the Earth's atmosphere contains 21% oxygen and most of the oceans are well-oxygenated. However, for most of our planet's 4567 million year (Myr) long history, it was not this way. Our reading of the rock record paints a picture of protracted oxygenation of the atmosphere and oceans (Figure 1). For more than 2000 million years (Myr) after Earth's formation, free O2 was almost non-existent at the Earth's surface and the oceans were predominantly Fe2+-rich. Oxygen did not begin to accumulate in the atmosphere until 2400-2100 Myr ago – a time interval called the "Great Oxidation Event". During this event, it is estimated that atmospheric O2 concentrations rose to a level equivalent to about 1-10% of today.
Figure 1. Earth's surface oxygenation through time and its relationship to significant steps in biological evolution.

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 O2-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.

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.

The Great Oxidation Event led to widespread oxygenation of the surface oceans. However, atmospheric O2 levels were not high enough to oxygenate the deep oceans. Instead, the Earth's oceans became stratified, with oxygenated surface waters, anoxic and H2S-rich (sulfidic) middle waters, and anoxic and Fe2+-bearing (ferruginous) deep waters. How did the sulfidic conditions originate? In the presence of O2, sulfide minerals exposed on land would be oxidized to sulfate, which was then delivered to the oceans by rivers. In coastal regions where large amounts of dead organic matter from primary producers were sinking from the surface ocean, bacteria obtained energy by oxidizing the organic matter while reducing sulfate to sulfide. Sulfidic conditions then arose when enough H2S was produced to consume all O2 in the middle water column.
Widespread ocean redox stratification likely persisted for more than 1500 Myr of Earth's middle age. However, this period of time was not entirely monotonic. The younger part of the Great Oxidation Event features a transient rise in atmospheric O2 levels 2200-2100 Myr ago. A possible explanation is that the onset of global oxidative continental weathering delivered a large load of phosphorus to the oceans, triggering massive primary productivity and burial of organic matter in sediments. By contrast, a temporary fall in ocean O2 levels occurred 1900 Myr ago because intense volcanism released large amounts of Fe2+ and other reductants. Afterwards, there appears to have been relatively little change in atmosphere-ocean oxygenation for a long time. During this "boring" billion-year-long interval, eukaryotic evolution proceeded very slowly.
In stark contrast, the interval between 800 and 500 Myr ago was marked by dramatic changes, specifically a major oxygenation event, breakup of a supercontinent, at least two severe glaciations, and major eukaryotic diversification. Formation and breakup of a tropical supercontinent supplies abundant nutrients to the oceans and may have led to high rates of primary productivity and organic matter burial. Newly evolved marine eukaryotes with organic body parts more resistant to degradation could also have allowed more efficient organic matter burial. However, the greatest driving force for change may have been the glaciations (Figure 3). In the wake of the youngest global glaciation 635 Myr ago (a "Snowball Earth"), a hot climate likely promoted elevated primary productivity and organic matter burial. A significant increase in ocean oxygenation followed shortly after the glaciation.
Figure 3. Glacial sediments deposited ~670 million years ago in an ocean basin.

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.

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.

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.

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).

Armed with these tools, geoscientists will continue to probe the Earth's rock record and provide us with the necessary knowledge to ensure that we are best equipped to deal with the environmental threats facing us, and to guide us on the search for life elsewhere in the cosmos. The story of oxygen on Earth is one aspect of the rapidly emerging field of astrobiology - which studies the origin, evolution, and distribution of life in the universe. Perhaps one day the astrobiologists will answer the one question at the back of all our minds: are we alone?
Selected (recent) papers and reviews on the history of Earth's surface oxygenation:
Anbar et al. (2007) Science 317, 1903-1906.
Bekker et al. (2004) Nature 427, 117-120.
Bekker and Holland (2012) Earth and Planetary Science Letters 317-318, 295-304.
Berner (2003) Nature 426, 323-326.
Brennecka et al. (2011) Proceedings of the National Academy of Sciences 108, 17631-17634.
Catling and Claire (2005) Earth and Planetary Science Letters 237, 1-20.
Cohen et al (2004) Geology 32, 157-160.
Dahl et al. (2010) Proceedings of the National Academy of Sciences 107, 17911-17915.
Falkowski and Godfrey (2008) Philosophical Transactions Royal Society B 363, 2705-2716.
Gaillard et al. (2011) Nature 478, 229-232.
Holland (2006) Philosophical Transactions Royal Society B 361, 903-915.
Holland (2009) Geochimica et Cosmochimica Acta 73, 5241-5255.
Kendall et al. (2010) Nature Geoscience 3, 647-652.
Och and Shields-Zhou (2012) Earth-Science Reviews 110, 26-57.
Poulton et al. (2010) Nature Geoscience 3, 486-490.
Planavsky et al. (2011) Nature 477, 448-451.
Rasmussen et al (2012) Nature 484, 498-501.
Turgeon and Creaser (2008) Nature 454, 323-326.
Sahoo et al. (2012) Nature 489, 546-549.
Scott et al. (2008) Nature 452, 456-459.