The Great Oxygenation Event

  • Roberto Ligrone


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.


  1. 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 358:267–274CrossRefGoogle Scholar
  2. Bekker A (2014a) Great oxygenation event. Encycl Astrobiol. Google Scholar
  3. Bekker A (2014b) Huronian glaciation. Encycl Astrobiol. Google Scholar
  4. Bekker A (2014c) Lomagundi carbon isotope excursion. Encycl Astrobiol. Google Scholar
  5. Belcher CM, McElwain JC (2008) Limits for combustion in low O2 redefine paleoatmospheric predictions for the Mesozoic. Science 321:1197–1200PubMedCrossRefGoogle Scholar
  6. Berner RA, VandenBrooks JM, Ward PD (2007) Oxygen and evolution. Science 316:557–558PubMedCrossRefGoogle Scholar
  7. Butterfield NJ (2011) Animals and the invention of the Phanerozoic earth system. Trends Ecol Evol 26:81–87PubMedCrossRefGoogle Scholar
  8. Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396:450–453CrossRefGoogle Scholar
  9. Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95PubMedCrossRefGoogle Scholar
  10. Catling DC, Claire MC (2005) How Earth’s atmosphere evolved to an oxic state: a status report. Earth Planet Sci Lett 237:1–20CrossRefGoogle Scholar
  11. 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 754–761CrossRefGoogle Scholar
  12. Catling DC, Zahnle KJ, McKay CP (2001) Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293:839–843PubMedCrossRefGoogle Scholar
  13. Catling DC, Claire MC, Zahnle KJ (2007) Anaerobic methanotrophy and the rise of atmospheric oxygen. Phil Trans R Soc A 365:1867–1888PubMedCrossRefGoogle Scholar
  14. Claire MW, Catling DC, Zahnle J (2006) Biogeochemical modeling of the rise of oxygen. Geobiology 4:239–269CrossRefGoogle Scholar
  15. Cole DB et al (2016) A shale-hosted Cr isotope record of low atmospheric oxygen during the Proterozoic. Geology 44:555–558CrossRefGoogle Scholar
  16. Crowe SA et al (2013) Atmospheric oxygenation three billion years ago. Nature 501:535–538PubMedCrossRefGoogle Scholar
  17. Crowe SA et al (2014) Deep-water anoxygenic photosythesis in a ferruginous chemocline. Geobiology 12:322–339PubMedCrossRefGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. Ducluzeau AL et al (2009) Was nitric oxide the first strongly oxidizing terminal electron sink? Trends Biochem Sci 34:9–15CrossRefGoogle Scholar
  20. Falkowski PG, Godfrey LV (2008) Electrons, life and the evolution of Earth’s oxygen cycle. Philos Trans R Soc B 363:2705–2716CrossRefGoogle Scholar
  21. Farquhar J, Bao H, Thiemans M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289:756–758PubMedPubMedCentralCrossRefGoogle Scholar
  22. Feulner G, Hallmann C, Kienert H (2015) Snowball cooling after algal rise. Nat Geosci 8:659–662CrossRefGoogle Scholar
  23. Gaillard F, Scaillet B, Arndt NT (2011) Atmospheric oxygenation caused by a change in volcanic degassing pressure. Nature 478:229–233PubMedCrossRefGoogle Scholar
  24. Goldblatt C, Lenton TM, Watson AJ (2006) Bistability of atmospheric oxygen and the great oxidation. Nature 443:683–686PubMedCrossRefGoogle Scholar
  25. Guo Q et al (2009) Reconstructing Earth’s surface oxidation across the Archean-Proterozoic transition. Geology 37:399–402CrossRefGoogle Scholar
  26. Hoffman PF, Schrag DP (2002) The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14:129–155CrossRefGoogle Scholar
  27. Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc B 361:903–915CrossRefGoogle Scholar
  28. Holland HD (2009) Why the atmosphere became oxygenated: a proposal. Geochim Cosmochim Acta 73:5241–5255CrossRefGoogle Scholar
  29. Jiang Y-Y et al (2012) The impact of oxygen on metabolic evolution: a chemoinformatic investigation. PLoS Comput Biol 8:e1002426. PubMedPubMedCentralCrossRefGoogle Scholar
  30. Johnson J et al (2014) O2 constraint from Paleoproterozoic detrital pyrite and uraninite. Geol Soc Am Bull 126:813–830CrossRefGoogle Scholar
  31. Kartal B et al (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37:428–461CrossRefGoogle Scholar
  32. Kasting JF (2013) What caused the rise of atmospheric O2? Chem Geol 342:13–25CrossRefGoogle Scholar
  33. Kluge M (1994) Geosiphon pyriforme (Kützing) von Wettstein, a promising system for studying endocyanoses. Prog Bot 55:130–141CrossRefGoogle Scholar
  34. Konhauser KO et al (2009) Oceanic nickel depletion and a methanogen famine before the great oxidation event. Nature 458:750–753PubMedCrossRefGoogle Scholar
  35. Konhauser KO et al (2011) Aerobic bacterial pyrite oxidation and acid rock drainage during the great oxidation event. Nature 478:369–373PubMedCrossRefGoogle Scholar
  36. 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 102:11131–11136PubMedPubMedCentralCrossRefGoogle Scholar
  37. Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278PubMedCrossRefGoogle Scholar
  38. Laakso T, Schrag D (2014) Regulation of atmospheric oxygen during the Proterozoic. Earth Planet Sci Lett 388:81–91CrossRefGoogle Scholar
  39. Laakso T, Schrag D (2017) A theory of atmospheric oxygen. Geobiology 15:366–384PubMedCrossRefGoogle Scholar
  40. Lalonde SV, Konhauser KO (2015) Benthic perspective on Earth’s oldest evidence for oxygenic photosynthesis. Proc Natl Acad Sci U S A 112:995–1000PubMedPubMedCentralCrossRefGoogle Scholar
  41. Lane N (2002) Oxygen, the molecule that made the world. Oxford University Press, OxfordGoogle Scholar
  42. Lenton T, Watson A (2011) Revolutions that made the Earth. Oxford University Press, OxfordCrossRefGoogle Scholar
  43. 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 112:8193–8198CrossRefGoogle Scholar
  44. Lyons TW et al (2009) Tracking euxinia in the ancient ocean: multiproxy perspective and Proterozoic case study. Annu Rev Earth Planet Sci 37:507–534CrossRefGoogle Scholar
  45. Lyons TW, Reinhard CT, Planavsky NJ (2014a) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315PubMedCrossRefGoogle Scholar
  46. Lyons TW, Reinhard CT, Planavsky NJ (2014b) Evolution: a fixed-nitrogen fix in the early ocean? Curr Biol 24:R276–R278PubMedCrossRefGoogle Scholar
  47. 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 358:59–85CrossRefGoogle Scholar
  48. Mentel M, Martin W (2008) Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos Trans R Soc B 363:2717–2729CrossRefGoogle Scholar
  49. Nelson DR (2013) A world of cytochrome P450s. Philos Trans R Soc B 368:20120430. CrossRefGoogle Scholar
  50. Nisbet EG, Ellen R, Nisbet R (2008) Methane, oxygen, photosynthesis, rubisco and the regulation of the air through time. Philos Trans R Soc B 363:2745–2754CrossRefGoogle Scholar
  51. 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 369–370:284–293CrossRefGoogle Scholar
  52. Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41PubMedCrossRefGoogle Scholar
  53. Planavsky NJ (2014) The elements of marine life. Nat Geosci 7:855–856CrossRefGoogle Scholar
  54. 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 109:18300–18305PubMedPubMedCentralCrossRefGoogle Scholar
  55. Planavsky NJ et al (2014) Low mid-proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346:635–638PubMedCrossRefGoogle Scholar
  56. Raymond J, Segré D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767PubMedPubMedCentralCrossRefGoogle Scholar
  57. Reinhard CT et al (2013) Proterozoic ocean redox and biogeochemical stasis. Proc Natl Acad Sci U S A 110:5357–5362PubMedPubMedCentralCrossRefGoogle Scholar
  58. Reinhard CT et al (2017) Evolution of the global phosphorus cycle. Nature 541:386–389PubMedCrossRefGoogle Scholar
  59. Sànchez-Baracaldo P, Ridgwell A, Raven JA (2014) A Neoproterozoic transition in the marine nitrogen cycle. Curr Biol 24:1–6CrossRefGoogle Scholar
  60. 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 110:1791–1796PubMedPubMedCentralCrossRefGoogle Scholar
  61. Schirrmeister BE, Gugger M, Donoghue PCJ (2015) Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58:769–785PubMedPubMedCentralCrossRefGoogle Scholar
  62. Schoepp-Cothenet B et al (2013) On the universal core of bioenergetics. Biochim Biophys Acta 1827:79–93PubMedCrossRefGoogle Scholar
  63. Scott C et al (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456–459PubMedCrossRefGoogle Scholar
  64. 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 110:12355–12360PubMedPubMedCentralCrossRefGoogle Scholar
  65. Smit MA, Mezger K (2017) Earth’s early O2 cycle suppressed by primitive continents. Nat Geosci 10:788–792CrossRefGoogle Scholar
  66. Tang H, Chen Y (2013) Global glaciations and atmospheric change at ca. 2.3 Ga. Geosci Front 4:583–596CrossRefGoogle Scholar
  67. 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 59:158–176PubMedCrossRefGoogle Scholar
  68. Trail D, Watson EB, Tailby ND (2011) The oxidation state of Hadean magmas and implications for early Earth’s atmosphere. Nature 480:79–82PubMedCrossRefGoogle Scholar
  69. Van der Giezen M, Lenton T (2012) The rise of oxygen and complex life. J Eukaryot Microbiol 59:111–113CrossRefGoogle Scholar
  70. Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. Encyclopedia of Life Sciences. Wiley.
  71. Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020PubMedCrossRefGoogle Scholar
  72. Zahnle KJ, Catling DC, Claire MW (2013) The rise of oxygen and the hydrogen hourglass. Chem Geol 362:26–34CrossRefGoogle Scholar
  73. Zhang S et al (2016) Sufficient oxygen for animal respiration 1,400 million years ago. Proc Natl Acad Sci U S A 113:1731–1736PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 754-761CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Roberto Ligrone
    • 1
  1. 1.Department of Environmental, Biological and Pharmaceutical Sciences and TechnologiesUniversity of Campania “Luigi Vanvitelli”CasertaItaly

Personalised recommendations