The story of O:
How did oxygen come to be the second most abundant gas on Earth?
Paul G. Falkowski
1
and Yukio Isozaki
2
1
Department of Earth and Planetary Sciences and Institute of Marine and Coastal
Sciences, Rutgers University, 71 Dudley Road, New Brunswick, NJ 08901, USA falko@imcs.rutgers.edu
2 Department of Earth Science & Astronomy, The University of Tokyo, 3-8-1 Komaba,
Meguro, Tokyo 153-8902, Japan isozaki@ea.c.u-tokyo.ac.jp
Planetary atmospheric gas composition reflects (bio)geochemical processes on its surface. Two gases overwhelmingly dominate Earth’s atmosphere: N
2 and O
2.
The former is primordial and its presence and abundance are not driven by biological processes. Indeed, N
2
is virtually inert and has an atmospheric lifetime on the order of ~
1 billion years ( 1 ). In contrast, O
2
is continuously produced biologically via the photobiological oxidation of H
2
O, a process 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 ( 2 ). Yet, despite the ~2500 ratio in lifetimes, O
2 came to comprise between ~ 10 and 30% of the atmospheric volume for the past several 500 million years ( 3, 4 ). How did O
2
, 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 ( 5 ). Here we briefly examine the story of
O.

How the Earth got water
O is produced as an element (not the gas O
2
) via the so-called “main line” reaction sequence from successive
4
He fusion reactions in hot stars ( 6 ). 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 comprise the fundamental minerals in mafic and felsic rocks, and with H to form water ( 7 ). 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 ( 8 ). Regardless, isotopic data suggest that Earth’s surface contained liquid water within ~200 million years following 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 O
2
.
How water is split.
Water can be oxidized to its component elements by high energy (UV) photons.
However, if significant amounts of O
2
are produced, stratospheric ozone accumulates and quenches this process; this negative feedback prevents O
2
from becoming an abundant gas solely via abiotic photochemical processes ( 10 ). The pattern of isotopic fractionation of sulfur suggests that Earth did not have a significant amount of ozone until between 2.4 and 2.3 billion years ago ( 11 ). Hence, although peroxides almost certainly formed on the planetary surface from the early Archean due to the photochemical oxidation of water, and consequently there was almost certainly a continuous flux of oxidant, this process

was not responsible for production of significant amounts of free O
2
in Earth’s atmosphere ( 12 ). The production of peroxides and the rapid escape of H
2
to space, did however, prevent Earth’s atmosphere from becoming strongly reducing, which had been the widely accepted model of early Earth in the middle of the 20 th
century ( 13 ). It is now generally accepted that the early atmosphere of Earth was “mildly” reducing (
14, 15 ).
While undoubtedly the trajectory for all terrestrial planets is from reducing to oxidizing conditions due to H
2
escape ( 16 ), the evolution of a biological process that could photochemically “split” (i.e., oxidize) water greatly accelerated the oxidation process.
The biological oxidation of water is driven by a single microbially-derived process, the evolution of which remains poorly understood ( 17, 18 ). It appears to have arisen once in a single clade of Bacteria, and was appropriated via a series of successive endosymbitotic events into a highly diverse group of eukaryotes including algae and higher plants ( 18 ). 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 oxidation reaction in biology, and critical details on how it works are still largely unknown. Regardless, O
2
is produced as a byproduct, leading to the reaction:
2H
2
O ---- 4 e + 4 H
+
+ O
2
This reaction is basically a biogeochemical half-cell; the protons and electrons generated are primarily used to reduce CO
2
to allow the growth of new cells (and hence the formation of organic matter):
CO
2
+ 4 e + 4 H
+
------ (CH
2
O) + H
2
O

On time scales of years to millennia, these reactions are closely coupled to the reverse process of respiration, such that net production of O
2
is virtually nil. That is, without burial of organic matter in Earth’s crust, there would be very little free O
2
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 organic carbon. By far, the major reservoir is the crust. The major mechanism for burial of organic matter is sedimentation and accretion onto cratons, and to a lesser extent subduction deep into the mantle. These processes are driven by tectonics; a process that is presently unique to Earth among the planets in our solar system.
Radiogenic heat in Earth’s core leads to a continuous cycle in which continents collide, merge, fracture, separate and form new ocean basins ( 19, 20 ). However, the ocean cannot expand forever; as the oceanic lithosphere (plate) moves away from mid-oceanic ridge it becomes cooler, denser, and eventually subducts under the craton and the ocean begins to close up once again. Eventually, the plate subducts, and a fraction of the organic matter buried in the sediments along the margins ( 21 ) is added to continents, forming coastal mountain chains, and thus future cratons. Indeed, unless organic matter stored in marine sediments is added to 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 ( 22 ). 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 2.3 billion years ago, the atmospheric concentrations were probably ~ 1% by volume, and the ocean interior was probably still anoxic ( 23 ). Large increases in atmospheric oxygen appear to have occurred much later.
The oxidation of the atmosphere appears to have gotten a boost towards the end of the Proterozoic eon, about 750 million years ago, when tectonic processes accelerated the burial of organic matter. As Earth’s interior gradually cooled, the geothermal gradient steadily decreased and reached a threshold where deep hydrous (OH-containing) minerals were subducted deep into the mantle at depths of 410-660 km ( 24 ). This process resulted in a massive transfer of surface water into mantle, which, in turn, slowly lowered sealevel by up to 600 m and was accompanied by extensive emergence of continents. The secular drop in sea level led to erosion of the newly exposed land masses and the concomitant production of huge volume of sediments along continental margins, which helped accelerate the burial of organic matter. The burial of large amounts of organic carbon in sediments in the late Proterozoic is mirrored in a significant rise in atmospheric oxygen concentration which is blamed for triggering the Cambrian explosion of metazoans ( 24, 25 ). Further increases in burial efficiency were biologically catalyzed by

the evolution of eukaryotic algae, in the Proterozoic, and much later by the rise of land plants, especially trees, in the Carboniferous.
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.
Photosynthetic carbon fixation strongly discriminates against
13
CO
2
, such that the resulting organic matter is 20 to 25 parts per thousand enriched in
12
CO
2
relative to the source carbon. In contrast, carbonates are formed by the precipitation of HCO
3
with Ca or
Mg, retain the isotopic signal of the source carbon (e.g., HCO
3 in the oceans). If photosynthesis exceeds respiration (implying burial of organic carbon),
12
C is removed from the atmospheric ocean pool, leaving
13
C enriched source carbon. Thus, the isotopic composition of carbon in carbonates can be used to track the extent to which organic matter becomes buried over geological time ( 26 ). 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. This period of Earth’s history witnessed O
2
concentrations as high as about 30% ( 3 ). By the end of the Triassic extinction, O
2
concentrations appear to have been significantly lower ( 27 ), perhaps even as low as 12%, but rose secularly in the ensuing 200 million years, to the current level of 21% ( 4 ). Perhaps surprisingly, however, it is very difficult to extract a long-term secular increase in
13
C 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 ( 28 ).
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 ( 3 ). 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 ( 29 ). 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 ( 28 ). 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 ( 30 ). 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.
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Figure 1. Legend goes here.