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The Great Oxygenation Event

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Abstract

Old sedimentary rocks record the history of oxygen in the form of redox-sensitive chemical species such as iron, uranium or cerium ions, and mass-independent fractionation of sulphur isotopes. These proxies show that oxygen became a stable component of the atmosphere around 2.4 GYA, a transition dubbed as the “Great Oxygenation Event” (GOE). Oxygenic photosynthesis is by far the main source of oxygen on Earth. Evidence for transient “oxygen oases” suggests that oxygenic photosynthesis appeared long before the GOE. Methane photolysis in the atmosphere was probably the main oxygen sink preventing stable oxygen accumulation before 2.4 GYA. Around this date, a change in planetary geochemistry permitted average oxygen concentration to rise above a threshold level of about 0.001%; the consequent formation of a thin ozone layer reduced methane photolysis and triggered the transition to an oxic atmosphere. The GOE was coeval with Huronian global glaciations, but the causal link between the two events is uncertain. Oxygen atmospheric concentration stabilized at a low level during most of the Proterozoic. A second rise in oxygen concentration, probably reflecting an increase in global productivity and organic carbon sequestration, started around 800 MYA. The oxygen level was at least 3% 570 MYA and probably exceeded 10% at the beginning of Phanerozoic, thus supporting the evolution of complex life. Water in the ocean depth remained largely anoxic until 600 MYA and accumulated sulphide from biogenic sulphate reduction (euxinic oceans). The GOE profoundly affected biochemistry by promoting the evolution of high energy-yielding aerobic respiration, aerobic lytotrophy and novel biosynthetic pathways involving P450 cytochromes.

The evolution of the Earth’s atmosphere is essentially the story of atmospheric oxygen. Virtually every realm of the Earth sciences, biology, geology, geochemistry, oceanography and atmospheric science, is needed to piece together an understanding of the history of oxygen.

Catling and Claire (2005)

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References

  • Baymann F et al (2003) The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes. Philos Trans R Soc B 358:267–274

    Article  CAS  Google Scholar 

  • Bekker A (2014a) Great oxygenation event. Encycl Astrobiol. https://doi.org/10.1007/978-3-642-27833-4_1752-4

    Google Scholar 

  • Bekker A (2014b) Huronian glaciation. Encycl Astrobiol. https://doi.org/10.1007/978-3-642-27833-4_742-4

    Google Scholar 

  • Bekker A (2014c) Lomagundi carbon isotope excursion. Encycl Astrobiol. https://doi.org/10.1007/978-3-642-27833-4_5127-1

    Google Scholar 

  • Belcher CM, McElwain JC (2008) Limits for combustion in low O2 redefine paleoatmospheric predictions for the Mesozoic. Science 321:1197–1200

    Article  CAS  PubMed  Google Scholar 

  • Berner RA, VandenBrooks JM, Ward PD (2007) Oxygen and evolution. Science 316:557–558

    Article  CAS  PubMed  Google Scholar 

  • Butterfield NJ (2011) Animals and the invention of the Phanerozoic earth system. Trends Ecol Evol 26:81–87

    Article  PubMed  Google Scholar 

  • Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396:450–453

    Article  CAS  Google Scholar 

  • Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95

    Article  CAS  PubMed  Google Scholar 

  • Catling DC, Claire MC (2005) How Earth’s atmosphere evolved to an oxic state: a status report. Earth Planet Sci Lett 237:1–20

    Article  CAS  Google Scholar 

  • Catling DC, Zahnle K (2003) Evolution of atmospheric oxygen. In: Holton J, Curry J, Pyle J (eds) Encyclopedia of atmospheric sciences. Academic Press, London, pp 754–761

    Chapter  Google Scholar 

  • Catling DC, Zahnle KJ, McKay CP (2001) Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293:839–843

    Article  CAS  PubMed  Google Scholar 

  • Catling DC, Claire MC, Zahnle KJ (2007) Anaerobic methanotrophy and the rise of atmospheric oxygen. Phil Trans R Soc A 365:1867–1888

    Article  CAS  PubMed  Google Scholar 

  • Claire MW, Catling DC, Zahnle J (2006) Biogeochemical modeling of the rise of oxygen. Geobiology 4:239–269

    Article  CAS  Google Scholar 

  • Cole DB et al (2016) A shale-hosted Cr isotope record of low atmospheric oxygen during the Proterozoic. Geology 44:555–558

    Article  CAS  Google Scholar 

  • Crowe SA et al (2013) Atmospheric oxygenation three billion years ago. Nature 501:535–538

    Article  CAS  PubMed  Google Scholar 

  • Crowe SA et al (2014) Deep-water anoxygenic photosythesis in a ferruginous chemocline. Geobiology 12:322–339

    Article  CAS  PubMed  Google Scholar 

  • Donnadieu Y, Goddéris Y, Le Hir G (2014) Neoproterozoic atmospheres and glaciation. In: Holland HD, Turekian KK (eds) Treatise on geochemistry, vol 6, 2nd edn. Elsevier, Oxford, pp 217–229. https://www.researchgate.net/publication/282074349

    Chapter  Google Scholar 

  • Ducluzeau AL et al (2009) Was nitric oxide the first strongly oxidizing terminal electron sink? Trends Biochem Sci 34:9–15

    Article  CAS  PubMed  Google Scholar 

  • Falkowski PG, Godfrey LV (2008) Electrons, life and the evolution of Earth’s oxygen cycle. Philos Trans R Soc B 363:2705–2716

    Article  CAS  Google Scholar 

  • Farquhar J, Bao H, Thiemans M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289:756–758

    Article  CAS  PubMed  Google Scholar 

  • Feulner G, Hallmann C, Kienert H (2015) Snowball cooling after algal rise. Nat Geosci 8:659–662

    Article  CAS  Google Scholar 

  • Gaillard F, Scaillet B, Arndt NT (2011) Atmospheric oxygenation caused by a change in volcanic degassing pressure. Nature 478:229–233

    Article  CAS  PubMed  Google Scholar 

  • Goldblatt C, Lenton TM, Watson AJ (2006) Bistability of atmospheric oxygen and the great oxidation. Nature 443:683–686

    Article  CAS  PubMed  Google Scholar 

  • Guo Q et al (2009) Reconstructing Earth’s surface oxidation across the Archean-Proterozoic transition. Geology 37:399–402

    Article  Google Scholar 

  • Hoffman PF, Schrag DP (2002) The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14:129–155

    Article  CAS  Google Scholar 

  • Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc B 361:903–915

    Article  CAS  Google Scholar 

  • Holland HD (2009) Why the atmosphere became oxygenated: a proposal. Geochim Cosmochim Acta 73:5241–5255

    Article  CAS  Google Scholar 

  • Jiang Y-Y et al (2012) The impact of oxygen on metabolic evolution: a chemoinformatic investigation. PLoS Comput Biol 8:e1002426. https://doi.org/10.1371/journal.pcbi.1002426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson J et al (2014) O2 constraint from Paleoproterozoic detrital pyrite and uraninite. Geol Soc Am Bull 126:813–830

    Article  CAS  Google Scholar 

  • Kartal B et al (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37:428–461

    Article  CAS  PubMed  Google Scholar 

  • Kasting JF (2013) What caused the rise of atmospheric O2? Chem Geol 342:13–25

    Article  Google Scholar 

  • Kluge M (1994) Geosiphon pyriforme (Kützing) von Wettstein, a promising system for studying endocyanoses. Prog Bot 55:130–141

    Article  Google Scholar 

  • Konhauser KO et al (2009) Oceanic nickel depletion and a methanogen famine before the great oxidation event. Nature 458:750–753

    Article  CAS  PubMed  Google Scholar 

  • Konhauser KO et al (2011) Aerobic bacterial pyrite oxidation and acid rock drainage during the great oxidation event. Nature 478:369–373

    Article  CAS  PubMed  Google Scholar 

  • Kopp RE et al (2005) The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci U S A 102:11131–11136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278

    Article  CAS  PubMed  Google Scholar 

  • Laakso T, Schrag D (2014) Regulation of atmospheric oxygen during the Proterozoic. Earth Planet Sci Lett 388:81–91

    Article  CAS  Google Scholar 

  • Laakso T, Schrag D (2017) A theory of atmospheric oxygen. Geobiology 15:366–384

    Article  CAS  PubMed  Google Scholar 

  • Lalonde SV, Konhauser KO (2015) Benthic perspective on Earth’s oldest evidence for oxygenic photosynthesis. Proc Natl Acad Sci U S A 112:995–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane N (2002) Oxygen, the molecule that made the world. Oxford University Press, Oxford

    Google Scholar 

  • Lenton T, Watson A (2011) Revolutions that made the Earth. Oxford University Press, Oxford

    Book  Google Scholar 

  • Li W, Beard BL, Johnson CM (2015) Biologically recycled continental iron is a major component in banded iron formations. Proc Nat Acad Sci U S A 112:8193–8198

    Article  CAS  Google Scholar 

  • Lyons TW et al (2009) Tracking euxinia in the ancient ocean: multiproxy perspective and Proterozoic case study. Annu Rev Earth Planet Sci 37:507–534

    Article  CAS  Google Scholar 

  • Lyons TW, Reinhard CT, Planavsky NJ (2014a) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315

    Article  CAS  PubMed  Google Scholar 

  • Lyons TW, Reinhard CT, Planavsky NJ (2014b) Evolution: a fixed-nitrogen fix in the early ocean? Curr Biol 24:R276–R278

    Article  CAS  PubMed  Google Scholar 

  • Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc B 358:59–85

    Article  CAS  Google Scholar 

  • Mentel M, Martin W (2008) Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos Trans R Soc B 363:2717–2729

    Article  Google Scholar 

  • Nelson DR (2013) A world of cytochrome P450s. Philos Trans R Soc B 368:20120430. https://doi.org/10.1098/rstb.2012.0430

    Article  Google Scholar 

  • Nisbet EG, Ellen R, Nisbet R (2008) Methane, oxygen, photosynthesis, rubisco and the regulation of the air through time. Philos Trans R Soc B 363:2745–2754

    Article  CAS  Google Scholar 

  • Partin CA et al (2013) Large-scale fluctuations in Precambrian atmospheric and oceanic oxygen levels from the record of U in shales. Earth Planet Sci Lett 369–370:284–293

    Article  Google Scholar 

  • Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41

    Article  CAS  PubMed  Google Scholar 

  • Planavsky NJ (2014) The elements of marine life. Nat Geosci 7:855–856

    Article  CAS  Google Scholar 

  • Planavsky NJ et al (2012) Sulfur record of rising and falling marine oxygen and sulfate levels during the Lomagundi event. Proc Natl Acad Sci U S A 109:18300–18305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Planavsky NJ et al (2014) Low mid-proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346:635–638

    Article  CAS  PubMed  Google Scholar 

  • Raymond J, Segré D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767

    Article  CAS  PubMed  Google Scholar 

  • Reinhard CT et al (2013) Proterozoic ocean redox and biogeochemical stasis. Proc Natl Acad Sci U S A 110:5357–5362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhard CT et al (2017) Evolution of the global phosphorus cycle. Nature 541:386–389

    Article  CAS  PubMed  Google Scholar 

  • Sànchez-Baracaldo P, Ridgwell A, Raven JA (2014) A Neoproterozoic transition in the marine nitrogen cycle. Curr Biol 24:1–6

    Article  Google Scholar 

  • Schirrmeister BE et al (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc Natl Acad Sci U S A 110:1791–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schirrmeister BE, Gugger M, Donoghue PCJ (2015) Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58:769–785

    Article  PubMed  PubMed Central  Google Scholar 

  • Schoepp-Cothenet B et al (2013) On the universal core of bioenergetics. Biochim Biophys Acta 1827:79–93

    Article  CAS  PubMed  Google Scholar 

  • Scott C et al (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456–459

    Article  CAS  PubMed  Google Scholar 

  • Shih PM, Matzkeb NJ (2013) Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci U S A 110:12355–12360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smit MA, Mezger K (2017) Earth’s early O2 cycle suppressed by primitive continents. Nat Geosci 10:788–792

    Article  CAS  Google Scholar 

  • Tang H, Chen Y (2013) Global glaciations and atmospheric change at ca. 2.3 Ga. Geosci Front 4:583–596

    Article  CAS  Google Scholar 

  • Tomiki T, Saitou N (2004) Phylogenetic analysis of proteins associated in the four major energy metabolism systems: photosynthesis, aerobic respiration, denitrification, and sulfur respiration. J Mol Evol 59:158–176

    Article  CAS  PubMed  Google Scholar 

  • Trail D, Watson EB, Tailby ND (2011) The oxidation state of Hadean magmas and implications for early Earth’s atmosphere. Nature 480:79–82

    Article  CAS  PubMed  Google Scholar 

  • Van der Giezen M, Lenton T (2012) The rise of oxygen and complex life. J Eukaryot Microbiol 59:111–113

    Article  Google Scholar 

  • Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. Encyclopedia of Life Sciences. Wiley. www.els.net

  • Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020

    Article  CAS  PubMed  Google Scholar 

  • Zahnle KJ, Catling DC, Claire MW (2013) The rise of oxygen and the hydrogen hourglass. Chem Geol 362:26–34

    Article  CAS  Google Scholar 

  • Zhang S et al (2016) Sufficient oxygen for animal respiration 1,400 million years ago. Proc Natl Acad Sci U S A 113:1731–1736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catling D, Zahnle K (2003) Evolution of atmospheric oxygen. In: Holton J, Curry J, Pyle J (eds) Encyclopedia of Atmospheric Sciences. Academic Press, London, UK, p 754-761

    Chapter  Google Scholar 

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Ligrone, R. (2019). The Great Oxygenation Event. In: Biological Innovations that Built the World. Springer, Cham. https://doi.org/10.1007/978-3-030-16057-9_5

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