The biological and geological contingencies for th

Authors: Paul G Falkowski

Publish Date: 2010/12/29

Volume: 107, Issue: 1, Pages: 7-10

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Abstract

Oxygen is the third most abundant element in our solar system Atomic oxygen is formed along the socalled ‘main line’ sequence from the hightemperature fusion of four 4He 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 46 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 galaxyMolecular orbital calculations reveal that the atom has six valence electrons a valence of two and naturally forms a diradical molecule with one σ and one π bond and two unpaired electrons in degenerate lower antibonding 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 NO x PO4 and SO x 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 2008Earth 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 nonequilibrium condition is the photosynthetic transduction of solar energy to chemical bond energyOver the past ~24 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 × 1018 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 of the atmosphere and without oxygen complex animal life could not have arisen In this special issue of Photosynthesis Research we explore hypotheses related to the evolution of oxygenic photosynthesis the geochemical evidence for the oxidation of Earth’s atmosphere and the consequences of the altered redox state to the Earth system including the evolution of animal lifeAll oxygenic photosynthetic organisms are derived from a single common ancestor the origin of which remains obscure Falkowski and Knoll 2007 The contemporary manifestation of this metabolic pathway in prokaryotes is restricted to a single taxa cyanobacteria All cyanobacteria contain two photochemical reaction centers one which oxidizes water the second reduces ferredoxin Despite large differences in the prosthetic groups and primary amino acid sequences between the two reaction centers their molecular architecture is remarkably similar While the two reaction centers appear to have originated from two extant clades of photosynthetic bacteria molecular phylogeny and structural information suggest the two reaction centers themselves originated from a common ancestor and diverged long before the origin of oxygenic photosynthesis Sadekar et al 2006 How and when the genes were transferred and mutated to yield an oxygenic photochemical apparatus is not clear It is clear however that the manganese/calcium oxide cluster on the luminal side of photosystem II and the four light driven electron transfer reactions leading to the production of each O2 molecule is unique in biology The structure and evolution of PSII is discussed by Hiller and his group Williamson et al 2010 and the timing of the appearance of cyanobacteria in the fossil record is discussed by Schopf 2010 The latter examines the data for both morphological fossils or “cellular” fossils as well as molecular fossils and isotopic measurementsThe oldest known rocks from which one potentially could infer early photosynthetic processes are from the Isua formation in southwest Greenland Because of glacial scouring in the recent geological past outcrops of these metamorphic rocks of clear sedimentary source are easily accessed but because of post depositional heating they contain no morphological fossils However carbon in the form of graphite from these rocks formed ~38 Ga billion years ago is isotopically depleted in 13C strongly suggesting that the carbon was biologically derived from a photosynthetic pathway Further geochemical evidence of molecular biomarkers and morphological fossils suggest that cyanobacteria could have evolved as early as 32 Ga or as late as 245 Ga however it seems that by about 24 Ga sufficient oxygen accumulated in Earth’s atmosphere to lead to the formation of stratospheric ozoneThe inference of ozone and the timing of this socalled “great oxidation event” GOE at 24 Ga comes primarily from analyses of sulfur isotopes in the rock record The analyses and the interpretation described by Farquhar et al 2010 is based on the mass independent isotopic fractionation of sulfur Basically there are four stable sulfur isotopes 32S 33S 34S and 36S Virtually all reactions that involve formation or the breaking of chemical bonds among these isotopes is massdependent that is the isotope with the smaller mass is reactive has a higher zero point kinetic energy and the resulting products are predicted from first principles to be enriched in the lighter isotope However up until ~24 Ga the isotopic fractionations in the geologic record are mass independent SO2 has a UV absorption cross section peaking at ~200 nm Breaking of bonds by high energy photons does not lead to mass dependent isotopic fractionation Hence one interpretation of the mass independent fractionation is that short wave UV radiation reached the Earth’s surface prior to ~24 Ga but subsequently that radiation was quenched Stratospheric ozone absorbs short wave UV radiation on the contemporary Earth and the source of ozone is O2 Hence the loss of the mass independent isotopic fractionation of sulfur at 24 Ga suggests a change in the oxidation state of Earth’s atmosphere The mass independent fractionation signal for S never returned and hence it is concluded that the transition from an anaerobic world to an oxidized world occurred once and only once in Earth’s history It should be noted that the concentration of oxygen that arose during the GOE is extremely poorly constrained Formation of stratospheric ozone is not limited by O2 above ca 01 of the present atmospheric level Geochemists use other proxies including N isotopes Godfrey and Falkowski 2009 transition metal composition and isotopic values Kaufman et al 2007 and even mineral composition Hazen et al 2008 to further attempt to constrain the concentration of oxygen during the GOE and to understand what controlled the net accumulation of the gas over the ensuing 23 billion yearsHigh concentrations of free molecular oxygen in a planetary atmosphere cannot come about simply by high energy photolysis of water that reaction is self quenching as UV becomes increasingly blocked Further as in all redox reactions a reductant the equivalent of hydrogen is formed To bring about a change in the oxidation state of the atmosphere the redox reactions cannot be at equilibrium but rather the reductant has to be removed and stored for long periods of geological time Hence the evolution of oxygenic photosynthesis was a necessary but not sufficient condition for the oxidation of the planetary surface

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