The Story of O2

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Science  24 Oct 2008:
Vol. 322, Issue 5901, pp. 540-542
DOI: 10.1126/science.1162641

Two gases overwhelmingly dominate Earth's atmosphere: N2 and O2. The former is primordial, and its presence and abundance are not driven by biological processes. Indeed, N2 is virtually inert and has an atmospheric lifetime on the order of 1 billion years (1). In contrast, O2 is continuously produced biologically via the oxidation of water driven by energy from the Sun. The gas was almost certainly virtually nonexistent in Earth's early atmosphere, is highly reactive, and has an atmospheric lifetime of ∼4 million years (2). Yet despite this comparatively short atmospheric lifetime, O2 came to constitute ∼10 to 30% of the atmospheric volume for the past ∼500 million years (3, 4).

How did O2, a gas critical to the evolution of animal life, become the second most abundant gas on Earth? The story is not as simple as it might first appear (5, 6). To understand it, we must know not only how and when O2 was first generated, but also how it came to persist in high concentrations in the atmosphere.

Elemental oxygen (O) is produced via the so-called “main line” nuclear reaction sequence from successive 4He fusion reactions in hot stars. It was delivered to the early Earth chemically bound to other elements. Through successive cycles of heating and cooling, O reacted with Si and C to form two of the major anions that, together with metal cations, constitute the fundamental minerals in mantle and crust, and with H to form water (7). Additional water was delivered to the planetary surface via meteorites and possibly comets; however, the relative proportions of the three sources are not well known (8). Regardless of the source, isotopic data suggest that Earth's surface contained liquid water within ∼200 million years after the accretion of the planet (9). Liquid water is a necessary condition for life as we know it, but it is not a sufficient condition for the biological production of O2.

Although water can be oxidized to its component elements by ultraviolet light, this reaction can produce only extremely small concentrations of O2 because of strong negative feedbacks (10). The overwhelming source of O2 on Earth is photobiological oxidation of water; neither the evolution nor the mechanism of this process are completely understood (11, 12). Apparently it arose once in a single clade of bacteria and was then appropriated via a single event, in which one cell engulfed another (endosymbiosis) to form a new symbiotic organism. The latter became the progenitor of all photosynthetic eukaryotes, including algae and higher plants (12).

The core of the oxidation machinery is photosystem II, a large protein complex containing four manganese atoms that are photocatalytically oxidized to create electron holes upstream. O2 is produced as a waste product via the reaction

2H2O → 4e + 4H+ + O2

The protons and electrons generated are used to reduce CO2 to form organic matter via

CO2 + 4e + 4H+ → (CH2O) + H2O

On time scales of years to millennia, these reactions are closely coupled to the reverse process of respiration, such that net production of O2 is virtually nil. That is, without burial of organic matter in rocks, there would be very little free O2 in the atmosphere. Hence, the evolution of oxygenic photosynthesis was a necessary but not a sufficient condition to oxidize Earth's atmosphere.

Processes controlling the flux and accumulation of O2 on Earth.

Water is photobiologically split with solar energy by algae in the ocean and plants on land. A very small fraction of the organic matter produced by these organisms is buried in sediments, and ultimately tectonically added to continents and subducted deep into Earth's mantle, thereby permitting O2 levels to accumulate in the atmosphere. The balance between burial of organic matter and its oxidation appears to have been tightly controlled over the past 500 million years.


Net oxidation of the atmosphere requires long-term storage of the reductants, primarily as organic carbon. The largest reservoir, by far, is Earth's crust. The major mechanism for burial of organic matter is sedimentation and accretion onto cratons (stabilized continents) and, to a lesser extent, subduction deep into the mantle (see the figure). These processes are driven by plate tectonics, in which radiogenic heat in Earth's interior drives mantle convection, allowing continents to collide and separate to form new ocean basins. During these cyclical collisions and separations, oceanic plates are eventually subducted under continents, and a fraction of the organic matter buried in the sediments is tectonically added to the continent, forming coastal mountain belts and thus increasing continental mass. Indeed, unless a large fraction of the organic matter stored in marine sediments is stabilized in cratons, it will be subducted, heated, and in part recharged to the atmosphere via volcanism, where it would become reoxidized (13, 14).

Thus, burial of organic matter, which contains reducing equivalents derived from the biological oxidation of water, implies a net oxidation of the atmosphere. The presence of O2 in the atmosphere requires an imbalance between oxygenic photosynthesis and aerobic respiration on time scales of millions of years; hence, to generate an oxidized atmosphere, more organic matter must be buried than respired.

How well do we know the concentration of O2 in Earth's atmosphere over geological time? Perhaps surprisingly, not very well. The major tool for quantitative reconstruction of the oxidation state of the planet is based on isotopic analysis of carbon in carbonates, and, to a lesser extent, sulfur in various mineral phases (3). Photosynthetic carbon fixation strongly discriminates against 13CO2, such that the resulting organic matter is enriched in 12CO2 relative to the source (mantle) carbon. In contrast, carbonates, formed by the precipitation of HCO3 - in seawater with Ca2+ and Mg2+, retain the isotopic signal of the source carbon. If photosynthesis exceeds respiration (implying burial of organic carbon), 12C is removed from the mobile pool of carbon in the atmosphere and oceans, leaving a 13C-enriched carbon source for biological and geochemical processes. Thus, the isotopic composition of carbon in carbonates can be used to track the extent to which organic matter was buried and was returned to the mobile pools over geological time (3, 15).

Although the initial oxidation of the atmosphere appears to have occurred about 2.2 billion years ago, atmospheric O2 concentrations were probably ∼1% of the present atmospheric level or less, and the deep ocean was likely still anoxic (16, 17). Large increases in atmospheric O2 appear to have occurred much later in Earth history, in the late Neoproterozoic (∼750 to 550 million years ago) and the Carboniferous (360 to 300 million years ago).

The boost in O2 inferred in the Neoproterozoic, inferred from carbon isotopic data, corresponds biologically to a rise in ecological prominence of large, single-celled eukaryotic algae (12)—that is, phytoplankton—which would have greatly accelerated the burial of organic matter in marine sediments, as well as geophysical controls resulting from mantle cooling and enhanced subduction. Metamorphic rock records through history suggest that heat flow from Earth's interior decreased steadily as the planet gradually cooled, and the geothermal gradient reached a threshold where hydrous (OH-containing) minerals were subducted deeper into the mantle (18). This process would have led to a massive transfer of surface water into mantle, potentially accelerating the extensive emergence of continents. This hypothesis is further supported by the historical record of oxygen isotopes (19).

The burial of large amounts of organic carbon over the past 750 million years is mirrored in a substantial rise in atmospheric O2, which may have triggered the Cambrian explosion of animal life (18, 20). Further increases in burial efficiency were accelerated in the Carboniferous (350 to 300 million years ago), as land plants, especially trees, came to double the primary productivity of the planet (3). Indeed, models based on the isotopic record of carbon and sulfur suggest that this period of Earth's history witnessed O2 concentrations as high as ∼30% (3). A very small fraction of the buried marine and terrestrial carbon was preserved as natural gas, petroleum, and coal. Currently, humans extract these resources at a rate about 1 million times the rate at which they were deposited in the lithosphere.

By the end of the Triassic extinction, O2 concentrations appear to have been much lower (21), perhaps even as low as 10 to 12% (3, 4). Over the past 200 million years, O2 concentrations have varied from ∼10% at the low end to as much as 23% at the high end (4). The relatively narrow range of variability suggests tight controls on the rate of burial and oxidation of organic matter on Earth's surface. Indeed, existing data do not show a long-term nonperiodic increase in 13C in carbonates over the past 2 billion years, implying that the reservoir of inorganic carbon in Earth's mantle is extremely large relative to the fraction of organic carbon buried, and that the burial of organic carbon is roughly balanced by oxidation and weathering.

This brief exploration shows that we understand in broad terms how O2 came to form a substantial part of Earth's atmosphere, but many details remain sketchy. We still do not understand the mechanism responsible for water splitting in oxygenic photosynthesis, nor do we know what controls the concentration of the gas in our planetary atmosphere (6, 13). The former issue should be resolved within a decade with the aid of high-resolution structures of the photosystems and sophisticated biophysical approaches to measuring electron transfer reactions (22). The latter issue will be more difficult to constrain, but a better understanding will emerge from more complete models coupled with better-integrated biogeochemical measurements (15).

Each mole of oxygen in Earth's atmosphere required ∼450 kJ equivalents of photon energy to produce. Given a concentration of ∼4 × 1019 moles of O2 in the contemporary atmosphere, the reservoir of the gas represents a staggering 2 × 1010 TJ hydrogen bomb equivalents of energy that is replaced every ∼4 million years. Nature certainly has provided an incredible source of potential energy for the evolution of life on Earth.


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