The Continuing Puzzle of the Great Oxidation Event

The rise of atmospheric O(2) was a milestone in the history of life. Although O(2) itself is not a climate-active gas, its appearance would have removed a methane greenhouse present on the early Earth and potentially led to dramatic cooling. Moreover, by fundamentally altering the biogeochemical cycles of C, N, S and Fe, its rise first in the atmosphere and later in the oceans would also have had important indirect effects on Earth's climate. Here, we summarize major lines of evidence from the geological literature that pertain to when and how O(2) first appeared in significant amounts in the atmosphere. On the early Earth, atmospheric O(2) would initially have been very low, probably <10(-5) of the present atmospheric level. Around 2.45 billion years ago, atmospheric O(2) rose suddenly in what is now termed the Great Oxidation Event. While the rise of oxygen has been the subject of considerable attention by Earth scientists, several important aspects of this problem remain unresolved. Our goal in this review is to provide a short summary of the current state of the field, and make the case that future progress towards solving the riddle of oxygen will benefit greatly from the involvement of molecular biologists.

[1]  Jennifer M. Robinson,et al.  PHANEROZOIC ATMOSPHERIC OXYGEN , 2003 .

[2]  O. Deux,et al.  The Story of O2 , 1990, IEEE Trans. Knowl. Data Eng..

[3]  R. Seifert,et al.  Biosynthesis of hopanoids by sulfate-reducing bacteria (genus Desulfovibrio). , 2006, Environmental microbiology.

[4]  W. Seyfried,et al.  Hydrothermal Fe fluxes during the Precambrian: Effect of low oceanic sulfate concentrations and low hydrostatic pressure on the composition of black smokers [rapid communication] , 2005 .

[5]  A. Schimmelmann,et al.  Fractionation of hydrogen isotopes in lipid biosynthesis , 1999 .

[6]  W. Martin,et al.  The hydrogen hypothesis for the first eukaryote , 1998, Nature.

[7]  G. Ourisson,et al.  HOPANOIDS. I: GEOHOPANOIDS : THE MOST ABUDANT NATURAL PRODUCTS ON EARTH ? , 1992 .

[8]  K. Bloch Sterol molecule: structure, biosynthesis, and function , 1992, Steroids.

[9]  R. Buick,et al.  Redox state of the Archean atmosphere: Evidence from detrital heavy minerals in ca. 3250–2750 Ma sandstones from the Pilbara Craton, Australia , 1999 .

[10]  K. Zahnle,et al.  Biogenic Methane, Hydrogen Escape, and the Irreversible Oxidation of Early Earth , 2001, Science.

[11]  R. Kopp,et al.  Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  S. Pääbo,et al.  Ancient DNA , 2001, Nature Reviews Genetics.

[13]  C. Walters,et al.  The Biomarker Guide , 2004 .

[14]  David C. Catling,et al.  The loss of mass‐independent fractionation in sulfur due to a Palaeoproterozoic collapse of atmospheric methane , 2006 .

[15]  K. Bloch Speculations on the evolution of sterol structure and function. , 1979, CRC critical reviews in biochemistry.

[16]  Abigail C. Allwood,et al.  Stromatolite reef from the Early Archaean era of Australia , 2006, Nature.

[17]  D. Segrè,et al.  Supporting Online Material Materials and Methods Tables S1 and S2 References the Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life , 2022 .

[18]  J. Kasting,et al.  Life and the Evolution of Earth's Atmosphere , 2002, Science.

[19]  G. Eglinton,et al.  Exploiting the multivariate isotopic nature of organic compounds , 2001 .

[20]  R. Kopp,et al.  The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Lowe,et al.  Hydrogen-based carbon fixation in the earliest known photosynthetic organisms , 2006 .

[22]  N. Pace A molecular view of microbial diversity and the biosphere. , 1997, Science.

[23]  D. D. Marais Isotopic Evolution of the Biogeochemical Carbon Cycle During the Precambrian , 2001 .

[24]  John P. Grotzinger,et al.  An abiotic model for stromatolite morphogenesis , 1996, Nature.

[25]  A. Pearson,et al.  Hypotheses for the origin and early evolution of triterpenoid cyclases , 2007, Geobiology.

[26]  H. D. Holland,et al.  The oxygenation of the atmosphere and oceans , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  J. Schopf,et al.  Microfossils of the Early Archean Apex Chert: New Evidence of the Antiquity of Life , 1993, Science.

[28]  J. Kasting,et al.  Rise of atmospheric oxygen and the “upside‐down” Archean mantle , 2001 .

[29]  Lee R. Kump,et al.  The rise of atmospheric oxygen , 2008, Nature.

[30]  L. Kump,et al.  Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago , 2007, Nature.

[31]  J. Kirschvink,et al.  Paleoproterozoic snowball earth: extreme climatic and geochemical global change and its biological consequences. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. Ourisson,et al.  Distribution of Hopanoid Triterpenes in Prokaryotes , 1984 .

[33]  I. Campbell,et al.  Formation of supercontinents linked to increases in atmospheric oxygen , 2008 .

[34]  A. Knoll,et al.  An iron shuttle for deepwater silica in Late Archean and early Paleoproterozoic iron formation , 2006 .

[35]  Donald E. Canfield,et al.  The Archean sulfur cycle and the early history of atmospheric oxygen. , 2000, Science.

[36]  P. Valdes,et al.  Climate and climate change , 2009, Current Biology.

[37]  J. Volkman Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways , 2005 .

[38]  O. Deux,et al.  The story of O 2 , 1992 .

[39]  M. Potts,et al.  The ecology of cyanobacteria: their diversity in time and space (reviewed by T. Bailey Watts) , 2001 .

[40]  Philip M. Novack-Gottshall,et al.  Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity , 2009, Proceedings of the National Academy of Sciences.

[41]  P. Falkowski Tracing Oxygen's Imprint on Earth's Metabolic Evolution , 2006, Science.

[42]  J. Hayes,et al.  Compound-specific isotopic analyses: a novel tool for reconstruction of ancient biogeochemical processes. , 1990, Organic geochemistry.

[43]  R. Summons,et al.  Sedimentary Hydrocarbons, Biomarkers for Early Life , 2003 .

[44]  P. Berg,et al.  A Whiff of Oxygen Before the Great Oxidation Event , 2007 .

[45]  H. Frimmel Archaean atmospheric evolution: evidence from the Witwatersrand gold fields, South Africa , 2005 .

[46]  R. Johnson,et al.  Hypoxia: A key regulator of angiogenesis in cancer , 2007, Cancer and Metastasis Reviews.

[47]  D. Sumner,et al.  Late Archean molecular fossils from the Transvaal Supergroup record the antiquity of microbial diversity and aerobiosis , 2009 .

[48]  R. Seifert,et al.  Aerobic methanotrophy in the oxic-anoxic transition zone of the black sea water column , 2007 .

[49]  J. Schopf,et al.  Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. , 1987, Science.

[50]  H. D. Holland When did the Earth's atmosphere become oxic? A Reply , 1999 .

[51]  Cornelia I. Bargmann,et al.  Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue , 2004, Nature.

[52]  D. Newman,et al.  Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph , 2007, Proceedings of the National Academy of Sciences.

[53]  Roger E. Summons,et al.  2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis , 1999, Nature.

[54]  R. Epand,et al.  Lipid domains in bacterial membranes and the action of antimicrobial agents. , 2009, Biochimica et biophysica acta.

[55]  P. Falkowski,et al.  The Story of O2 , 2008, Science.

[56]  R. Summons,et al.  Biogeochemistry of the 1640 Ma McArthur River (HYC) lead-zinc ore and host sediments, Northern Territory, Australia , 2001 .

[57]  D. Abbott,et al.  Plume‐related mafic volcanism and the deposition of banded iron formation , 1999 .

[58]  I. Fletcher,et al.  Reassessing the first appearance of eukaryotes and cyanobacteria , 2008, Nature.

[59]  J. VandenBrooks,et al.  Oxygen and Evolution , 2007, Science.

[60]  J. Peter Gogarten,et al.  Whole-Genome Analysis of Photosynthetic Prokaryotes , 2002, Science.

[61]  Donald E. Canfield,et al.  Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies , 1996, Nature.

[62]  J. Hayes,et al.  Terminal Proterozoic reorganization of biogeochemical cycles , 1995, Nature.

[63]  R. Buick When did oxygenic photosynthesis evolve? , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  A. J. Kaufman,et al.  Late Archean Biospheric Oxygenation and Atmospheric Evolution , 2007, Science.

[65]  J. Kasting,et al.  Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. , 2002, Astrobiology.

[66]  D. Newman,et al.  Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria , 2005 .

[67]  Yumiko Watanabe,et al.  Anomalous Fractionations of Sulfur Isotopes During Thermochemical Sulfate Reduction , 2009, Science.

[68]  G. Ourisson,et al.  Prokaryotic hopanoids and other polyterpenoid sterol surrogates. , 1987, Annual review of microbiology.

[69]  D. Canfield THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels , 2005 .

[70]  C. McKay,et al.  Why O2 is required by complex life on habitable planets and the concept of planetary "oxygenation time". , 2005, Astrobiology.

[71]  R. Summons,et al.  Targeted genomic detection of biosynthetic pathways: anaerobic production of hopanoid biomarkers by a common sedimentary microbe , 2005 .

[72]  Donald E. Canfield,et al.  Isotopic evidence for microbial sulphate reduction in the early Archaean era , 2001, Nature.

[73]  A. J. Kaufman,et al.  Isotopic evidence for Mesoarchaean anoxia and changing atmospheric sulphur chemistry , 2007, Nature.

[74]  M. Rohmer,et al.  Prokaryotic triterpenoids. 1. 3 beta-Methylhopanoids from Acetobacter species and Methylococcus capsulatus. , 1985, European journal of biochemistry.

[75]  J. Hayes,et al.  An isotopic biogeochemical study of the Green River oil shale. , 1992, Organic geochemistry.

[76]  Roger E. Summons,et al.  Composition and syngeneity of molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Pilbara Craton, Western Australia , 2003 .

[77]  Heinrich D. Holland,et al.  Volcanic gases, black smokers, and the great oxidation event , 2002 .

[78]  J. William Schopf,et al.  The Fossil Record: Tracing the Roots of the Cyanobacterial Lineage , 2000 .

[79]  S. Airieau,et al.  Observation of wavelength‐sensitive mass‐independent sulfur isotope effects during SO2 photolysis: Implications for the early atmosphere , 2001 .

[80]  A. Bekker,et al.  Dating the rise of atmospheric oxygen , 2004, Nature.

[81]  G. Roe,et al.  THE EARLY HISTORY OF ATMOSPHERIC OXYGEN : Homage to , 2006 .

[82]  Timothy M. Lenton,et al.  Bistability of atmospheric oxygen and the Great Oxidation , 2006, Nature.

[83]  S. Mojzsis,et al.  Multiple sulfur isotopes from Paleoproterozoic Huronian interglacial sediments and the rise of atmospheric oxygen , 2007 .

[84]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[85]  J. Farquhar,et al.  Multiple sulfur isotopes and the evolution of the atmosphere , 2003 .

[86]  H. D. Holland,et al.  Paleosols and the evolution of atmospheric oxygen: a critical review. , 1998, American journal of science.

[87]  S. Brassell,et al.  The geochemistry of terpenoids and steroids. , 1983, Biochemical Society transactions.

[88]  J. Slotte,et al.  How the molecular features of glycosphingolipids affect domain formation in fluid membranes. , 2009, Biochimica et biophysica acta.

[89]  A. Knoll,et al.  The Geological Succession of Primary Producers in the Oceans , 2007 .

[90]  Donald E. Canfield,et al.  Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides , 2002, Nature.

[91]  David Wacey,et al.  A fresh look at the fossil evidence for early Archaean cellular life , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[92]  N. Lane Oxygen: The molecule that made the world , 2002 .

[93]  D. Canfield Biogeochemistry of Sulfur Isotopes , 2001 .

[94]  N. Arndt,et al.  Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event , 2009, Nature.

[95]  H. Volk,et al.  Biomarkers from Huronian oil-bearing fluid inclusions: An uncontaminated record of life before the Great Oxidation Event , 2006 .

[96]  J. Xiong Photosynthesis: what color was its origin? , 2007, Genome Biology.

[97]  R Buick,et al.  Archean molecular fossils and the early rise of eukaryotes. , 1999, Science.

[98]  M. Rosing,et al.  U-rich Archaean sea-floor sediments from Greenland – indications of >3700 Ma oxygenic photosynthesis , 2004 .

[99]  A. Knoll The geological consequences of evolution , 2003 .

[100]  R. Summons,et al.  Methylhopane biomarker hydrocarbons in Hamersley Province sediments provide evidence for Neoarchean aerobiosis , 2008 .

[101]  Jacob R Waldbauer,et al.  Steroids, triterpenoids and molecular oxygen , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[102]  H. Volk,et al.  Preservation of hydrocarbons and biomarkers in oil trapped inside fluid inclusions for >2 billion years , 2008 .

[103]  M. Strous,et al.  The occurrence of hopanoids in planctomycetes : Implications for the sedimentary biomarker record , 2004 .

[104]  R. Buick The antiquity of oxygenic photosynthesis: evidence from stromatolites in sulphate-deficient Archaean lakes. , 1992, Science.