The biological and geological contingencies for the rise of oxygen on Earth

Oxygen is the third most abundant element in our solar system. Atomic oxygen is formed along the so-called ‘main line’ sequence from the high-temperature fusion of four He atoms in hot stars. Upon the explosion of the star at the end of its natural lifetime, the oxygen and other elements are redistributed and ultimately reaccreted to form new planets around a new sun. All oxygen on Earth was obtained during this accretion process approximately 4.6 billion years ago (Clayton 1993). The concentration of oxygen is approximately equal to or slightly higher than that of carbon in the solar atmospheres in this region of our galaxy. Molecular orbital calculations reveal that the atom has six valence electrons, a valence of two and naturally forms a diradical molecule with one r and one p bond and two unpaired electrons in degenerate lower (anti-bonding) orbitals; hence the ground state of molecular O2 is a triplet. This unusual electron configuration prevents O2 from reacting readily with atoms or molecules in a singlet configuration without forming radicals (Valentine et al. 1995); however, reactions catalyzed by metals or photochemical processes often lead to oxides of group I, II, III, IV, V and even VI elements spanning H2O, MgO and CaO, AlO, CO2, SiO2, NOx, PO4 and SOx. Oxygen also reacts with many trace elements, especially Mn and Fe, which in aqueous phase forms insoluble oxyhydroxides at neutral pH. The reactivity of oxygen is driven by electron transfer (redox) reactions, leading to highly stable products, such as H2O, CO2, HNO3, H2SO4 and H3PO4. The abiotic reactions of oxygen often involve unstable reactive intermediates such as H2O2, NO, NO2, CO and SO2. The reactions of oxygen with the other abundant light elements are almost always exergonic, meaning that, in contrast to N2, without a continuous source, free molecular oxygen would be depleted from Earth’s atmosphere within a few million years (Falkowski and Godfrey 2008). Earth is a unique planet in our solar system. Not only is it the only planet with both liquid water on its surface and sufficient radiogenic heat in its core to sustain plate tectonic processes, but its gas composition is far from thermodynamic equilibrium. Metaphorically the planet is similar to a gigantic biological cell. The analogue of a cell membrane is a thin film of crustal rock that separates the oxidized atmosphere on the outside from a reduced lithosphere on the inside. The energy sustaining this non-equilibrium condition is the photosynthetic transduction of solar energy to chemical bond energy. Over the past *2.4 billion years, oxygenic photosynthesis used liquid water as the dominant source of reductant, and carbon dioxide (or its hydrated equivalents) as the primary oxidant. The result over geological time has been the stable formation of molecular oxygen on the planetary surface. Indeed, at *4 9 10 mol, O2 is the second most abundant gas in Earth’s atmosphere. The origin, evolution, and mechanism of the water splitting reaction remain among the major unresolved questions in biology. However, although the photobiological splitting of water allowed for oxygenation of the atmosphere, geological processes were also critical; unless the reducing equivalents produced by photosynthetic organisms are buried in the lithosphere, there could not have been a net oxidation P. G. Falkowski (&) Environmental Biophysics and Molecular Ecology Program, Department of Earth and Planetary Sciences and Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901, USA e-mail: falko@marine.rutgers.edu