Perspective: the Rise of Oxygen on Earth

The story of O:

How did oxygen come to be the second most abundant gas on Earth?

Paul G. Falkowski1 and Yukio Isozaki2

1Department of Earth and Planetary Sciences and Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, NJ 088901, USA

2Department of Earth Science & Astronomy, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan

The gas composition on a planet reflects (bio)geochemical processes on its surface. 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 {Berner, 2006 #12694}. In contrast, O2 is continuously produced biologically via the oxidation of H2O driven by energy from the sun. The gas almost certainly was virtually nonexistent in Earth’s atmosphere when the planet was formed, is highly reactive, and has an atmospheric lifetime of ~ 4 million years {Keeling, 1993 #12695}. Yet, despite the ~250 ratio in atmospheric lifetimes, O2 came to comprise between ~ 10 and 30% of the atmospheric volume for the past several 500 million years {Berner, 2004 #102; Falkowski, 2005 #109}. How did O2, a gas critical to the evolution of animal life, become the second most abundant gas on Earth? The story isn’t as simple as it might first appear {Catling, 2005 #12141; Kump, 2008 #13008}. Here we briefly examine the story of O.

How the Earth got water

O is produced as an element (not the gas, O2) via the so-called “main line” reaction sequence from successive 4He fusion reactions in hot stars {Ziurys, 2007 #13014}. It is delivered to planets chemically bound to other elements. Through successive cycles of heating and cooling O reacts with Si and C to form two of the major anions that, together with metal cations, comprise the fundamental minerals in mantle and crust (ca. 80% of Earth’s volume), and with H to form water {Holland, 1984 #4786}. Additional water was also delivered to the planetary surface via meteriorites and possibly comets; however, the proportion of the three sources is not well constrained by H/D ratios in the contemporary ocean {Robert, 2001 #9125}. Regardless, isotopic data suggest that Earth’s surface contained liquid water within ~200 million years following the accretion of the planet {Mojzsis, 2001 #7367}. 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.

How water is split.

Although H2O can be oxidized to its component elements by high energy (UV) photons, this reaction can produce only extremely small concentrations of O2 because of strong negative feedbacks {Kasting, 1981 #13007}. By far, the overwhelming source of oxygen is the biological oxidation of water, driven by a single microbially-derived process, the evolution of which remains poorly understood {Blankenship #1336; Falkowski, 2007 #12961}. It appears to have arisen once in a single clade of Bacteria, and was appropriated via a single primary endosymbiotic event to become the progenator of all photosynthetic eukaryotes including algae and higher plants {Falkowski, 2007 #12961}. The core of the oxidation machinery is found in Photosystem II, a multimeric protein complex containing 4 Mn atoms which are successively oxidized by single, photocatalyzed reactions that create electron holes upstream. This is only known 4 electron transfer reaction in biology, and critical details on how it works are still unknown. Regardless, O2, produced as a waste product, via the reaction:

2H2O ---- 4 e + 4 H+ + O2

This reaction is basically a biogeochemical half-cell; the protons and electrons generated are primarily used to reduce CO2 to allow the growth of new cells (and hence the formation of organic matter):

CO2 + 4 e + 4 H+ ------(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 Earth’s rocks, there would be very little free O2 in the atmosphere. Hence, the evolution of oxygenic photosynthesis, the most complex energy transduction process in biology, was a necessary, but not sufficient condition to oxidize Earth’s atmosphere.

The improbability of tectonics

Net oxidation of the atmosphere requires long-term storage of the reductants, primarily as organic carbon. By far, the major reservoir is the 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. These processes are driven by plate tectonics; a process that is presently unique to Earth among the planets in our solar system. Radiogenic heat in Earth’s interior drives mantle convection allowing continents to collide and separate to form new ocean basins {Wilson, 1966 #215; Worsley, 1986 #152}. These collisions and separations are cyclical; the oceanic lithosphere (plate) moves away from mid-oceanic ridge and eventually subducts under the continent to close up the ocean once again. At the subduction margin, a fraction of the organic matter buried in the sediments {Premuzic, 1982 #8641} is tectonically added to continents, forming coastal mountain belts, i.e. increasing continental mass. Indeed, unless Oorganic matter stored in marine sediments is stabilzed in cratons, it will be subducted, heated, and in part recharged to the atmosphere via volcanism, where it would become reoxidized, or subducted much deeper into the mantle {Tappert, 2005 #13004}. Thus, burial of organic matter, which contains reducing equivalents derived from the biological oxidation of water, implies a net oxidation of the atmosphere. The basic concept is that oxygen 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. Although the oxidation of the atmosphere initially appears to have occurred about 2.2 billion years ago, probably by the rapid radiation of cyanobacteria and stabilization of the nitrogen cycle {Fennel, 2005 #12096}, the atmospheric concentrations were probably ~ 1% by volume or less, and the deep ocean was likely still anoxic {Canfield, 1998 #1859}. Large increases in atmospheric oxygen appear to have occurred much later.

The oxidation of the atmosphere may also have gotten a boost in the latest Precambrian age about 750 million years ago, when tectonic processes accelerated the burial of organic matter. Metamorphic rock records through history suggest that heat-flow from the Earth’s interior decreased steadily as the planet gradually cooled for nearly 4 billion years, and the geothermal gradient reached a threshold where hydrous (OH-containing) minerals were subducted deep into the mantle at depths of 410-660 km {Maruyama, 2005 #13013}. This process would have led to a massive transfer of surface water into mantle, which, in turn, slowly lowered sea-level (by up to 600 m, 25) and potentially accelerated extensive emergence of continents. The geotherm-induced first major sea level drop in history would lead to extensive continental erosion and the concomitant voluminous mass wasting along continental margins, which would, in turn, accelerate the burial of organic matter. The burial of large amounts of organic carbon over the past 750 million years is mirrored in a significant rise in atmospheric oxygen, which is often blamed for triggering the Cambrian explosion of metazoans {Knoll, 1999 #12208; Maruyama, 2005 #13013}. Further increases in burial efficiency were potentially accelerated by the evolution of large eukaryotic algae, in the Proterozoic which sink rapidly and become incorporated into sediments as organic matter, and much later by the rise of land plants, especially trees, in the Carboniferous. The former are major sources of petroleum and gas while the latter are sources of coal.

How well do we know the history of oxygen on Earth? Surprisingly perhaps, not very well. Most of inferences come from isotopic analyses, especially of carbon and sulfur {Berner, 2004 #102}. Photosynthetic carbon fixation strongly discriminates against 13CO2, such that the resulting organic matter is 20 to 25 parts per thousand enriched in 12CO2 relative to the source carbon. In contrast, carbonates, formed by the precipitation of HCO3 with Ca or Mg, retain the isotopic signal of the source carbon (e.g., HCO3 in seawaters). If photosynthesis exceeds respiration (implying burial of organic carbon), 12C is removed from the mobile pool of carbon in the atmosphere and oceans, leaving 13C enriched as a source of carbon 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 {Canfield, 2005 #13011}. This record reveals intervals of strong isotopic excursions and secular trends spanning hundreds of millions of years. One of these excursions occurred about 350 million years ago and corresponds to the rise of land plants in the Carboniferous. Models suggest that this period of Earth’s history witnessed O2 concentrations as high as about 30% {Berner, 2004 #102}. By the end of the Triassic extinction, O2 concentrations appear to have been significantly lower {Isozaki, 1997 #5139}, perhaps even as low as 12 to 15% {Falkowski, 2005 #109; Berner, 2006 #13010; Belcher, 2008 #13009}, but rose secularly in the ensuing 200 million years, to the current level of 21% {Falkowski, 2005 #109}. However, it is very difficult to observe a long-term secular 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 {Hayes, 2006 #12241}, and that the burial of organic carbon is roughly balanced by oxidation and weathering {Berner, 2004 #102}.

This very brief exploration of how oxygen came to be the second most abundant gas on this planet clearly shows the incredible contingencies required. Biological, geochemical and geophysical processes conspired to produce the planetary atmosphere that allows complex animal life to have evolved. Perhaps ironically, although it has been known for over 200 years that oxygenic photosynthesis is responsible for the production of oxygen, we still do not understand the basic mechanism responsible for water splitting, nor do we understand what controls the concentration of the gas in our planetary atmosphere {Berner, 2004 #102}. The former issue almost certainly will be resolved within a decade, as increasingly higher resolution structures of the photosystems become available, together with increasingly sophisticated biophysical approaches to measuring electron transfer reactions {Barber, 2008 #13006}. The latter issue will be more difficult to constrain, but a better understanding will emerge from more complete (not necessarily, complex) models coupled with better integrated biogeochemical measurements {Hayes, 2006 #12241}. We do know however, that the gas is not present in abundance on any other planet or their moons in our solar system. Hence, we left to search for the existence of life on those objects based on a compromise between our technological capabilities and our unfulfilled dreams of searching for proxy evidence. As technological capabilities develop, we can search for the existence of oxygen on planets outside of our solar system {Lawson, 2007 #13012}. While the identity of the gas on distant planets is difficult to confirm, it is a critical component in understanding how complex life can exist on Earth and how rare this planet really is.

References

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