Geological constraints on the origin of oxygenic photosynthesis
- 1.8k Downloads
- 90 Citations
Abstract
This article examines the geological evidence for the rise of atmospheric oxygen and the origin of oxygenic photosynthesis. The evidence for the rise of atmospheric oxygen places a minimum time constraint before which oxygenic photosynthesis must have developed, and was subsequently established as the primary control on the atmospheric oxygen level. The geological evidence places the global rise of atmospheric oxygen, termed the Great Oxidation Event (GOE), between ~2.45 and ~2.32 Ga, and it is captured within the Duitschland Formation, which shows a transition from mass-independent to mass-dependent sulfur isotope fractionation. The rise of atmospheric oxygen during this interval is closely associated with a number of environmental changes, such as glaciations and intense continental weathering, and led to dramatic changes in the oxidation state of the ocean and the seawater inventory of transition elements. There are other features of the geologic record predating the GOE by as much as 200–300 million years, perhaps extending as far back as the Mesoarchean–Neoarchean boundary at 2.8 Ga, that suggest the presence of low level, transient or local, oxygenation. If verified, these features would not only imply an earlier origin for oxygenic photosynthesis, but also require a mechanism to decouple oxygen production from oxidation of Earth’s surface environments. Most hypotheses for the GOE suggest that oxygen production by oxygenic photosynthesis is a precondition for the rise of oxygen, but that a synchronous change in atmospheric oxygen level is not required by the onset of this oxygen source. The potential lag-time in the response of Earth surface environments is related to the way that oxygen sinks, such as reduced Fe and sulfur compounds, respond to oxygen production. Changes in oxygen level imply an imbalance in the sources and sinks for oxygen. Changes in the cycling of oxygen have occurred at various times before and after the GOE, and do not appear to require corresponding changes in the intensity of oxygenic photosynthesis. The available geological constraints for these changes do not, however, disallow a direct role for this metabolism. The geological evidence for early oxygen and hypotheses for the controls on oxygen level are the basis for the interpretation of photosynthetic oxygen production as examined in this review.
Keywords
Oxygen evolution Atmospheric oxygenation Origin of photosynthesis Iron speciation Transition elements Isotopes Mass independent Sulfur isotopes Nitrogen metabolismNotes
Acknowledgments
The authors thank H. D. Holland, P. Falkowski, D. Catling, C. Reinhard, and an anonymous reviewer for constructive comments on the manuscript. The discussion of transition metal stable isotopes greatly benefited from comments and editing by S. Severmann. A. Bekker acknowledges support from an NSERC Discovery Grant. J. Farquhar acknowledges support from a NASA EXB grant and the NAI.
References
- Algeo TJ, Lyons TW (2006) Mo-total organic carbon covariation in modern anoxic marine environments: Implications for analysis of paleoredox and paleohydrographic conditions. Paleoceanography 21:PA1016Google Scholar
- Anbar AD, Rouxel O (2007) Metal stable isotopes in paleoceanography. Annu Rev Earth Planet Sci 35:717–746Google Scholar
- Anbar AD, Duan Y, Lyons TW, Arnold GL, Kendall B, Creaser RA, Kaufman AJ, Gordon GW, Scott C, Garvin J, Buick R (2007) A whiff of oxygen before the Great Oxidation Event? Science 317:1903–1906PubMedGoogle Scholar
- Arnold GL, Weyer S, Anbar AD (2004a) Fe isotope variations in natural materials measured using high mass resolution multiple collector ICPMS. Anal Chem 76:322–327PubMedGoogle Scholar
- Arnold GL, Anbar AD, Barling J, Lyons TW (2004b) Molybdenum isotope evidence for widespread anoxia in mid-proterozoic oceans. Science 304:87–90PubMedGoogle Scholar
- Aspler LB, Chiarenzelli JR, Bursey TL (1994) Ripple marks in quartz arenites of the Hurwitz group, Northwest-territories, Canada—evidence for sedimentation in a vast, early Proterozoic, shallow, fresh-water lake. J Sediment Res Sect A-Sediment Petrol Process 64:282–298Google Scholar
- Balan E, Cartigny P, Blanchard M, Cabaret D, Lazzeri M, Mauri F (2009) Theoretical investigation of the anomalous equilibrium fractionation of multiple sulfur isotopes during adsorption. Earth Planet Sci Lett 284:88–93Google Scholar
- Barley ME, Pickard AL, Sylvester PJ (1997) Emplacement of a large igneous province as a possible cause of banded iron formation 2.45 billion years ago. Nature 385:55–58Google Scholar
- Barley ME, Krapez B, Groves DI, Kerrich R (1998) The Late Archaean bonanza: metallogenic and environmental consequences of the interaction between mantle plumes, lithospheric tectonics, and global cyclicity. Precambrian Research 91:65–90Google Scholar
- Beal EJ, House CH, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187PubMedGoogle Scholar
- Beaumont V, Robert F (1999) Nitrogen isotope ratios of kerogens in Precambrian cherts: a record of the evolution of atmosphere chemistry? Precambr Res 96:63–82Google Scholar
- Beaumont VI, Jahnke LL, Des Marais DJ (2000) Nitrogen isotopic fractionation in the synthesis of photosynthetic pigments in Rhodobacter capsulatus and Anabaena cylindrica. Org Geochem 31:1075–1085Google Scholar
- Bekker A, Kaufman AJ (2007) Oxidative forcing of global climate change: a biogeochemical record across the oldest Paleoproterozoic ice age in North America. Earth Planet Sci Lett 258:486–499Google Scholar
- Bekker A, Kaufman AJ, Karhu JA, Beukes NJ, Swart QD, Coetzee LL, Eriksson KA (2001) Chemostratigraphy of the Paleoproterozoic Duitschland Formation, South Africa: implications for coupled climate change and carbon cycling. Am J Sci 301:261–285Google Scholar
- Bekker A, Holland HD, Wang PL, Rumble D, Stein HJ, Hannah JL, Coetzee LL, Beukes NJ (2004) Dating the rise of atmospheric oxygen. Nature 427:117–120PubMedGoogle Scholar
- Bekker A, Kaufman AJ, Karhu JA, Eriksson KA (2005) Evidence for Paleoproterozoic cap carbonates in North America. Precambr Res 137:167–206Google Scholar
- Bekker A, Karhu JA, Kaufman AJ (2006) Carbon isotope record for the onset of the Lomagundi carbon isotope excursion in the Great Lakes area, North America. Precambr Res 148:145–180Google Scholar
- Bekker A, Holmden C, Beukes NJ, Kenig F, Eglington B, Patterson WP (2008) Fractionation between inorganic and organic carbon during the Lomagundi (2.22–2.1 Ga) carbon isotope excursion. EPSL 271:278–291Google Scholar
- Bekker A, Barley ME, Fiorentini ML, Rouxel OJ, Rumble D, Beresford SW (2009) Atmospheric Sulfur in Archean Komatiite-Hosted Nickel Deposits. Science 326:1086–1089PubMedGoogle Scholar
- Bekker A, Slack JF, Planavsky N, Krapež B, Hofmann A, Konhauser KO, Rouxel OJ (2010) Iron formation: the sedimentary product of a complex interplay among mantle, tectonic, oceanic, and biospheric processes. Econ Geol 105:467–508Google Scholar
- Bertine KK, Turekian KK (1973) Molybdenum in marine deposits. Geochim Cosmochim Acta 48:605–615Google Scholar
- Beukes NJ, Klein C, Kaufman AJ, Hayes JM (1990) Carbonate petrography, kerogen distribution, and carbon and oxygen isotope variations in an early Proterozoic transition from limestone to iron-formation deposition, Transvaal Supergroup, South Africa. Econ Geol Bull Soc Econom Geol 85:663–690Google Scholar
- Buchachenko AL (1995) MIE versus CIE—comparative-analysis of magnetic and classical isotope effects. Chem Rev 95:2507–2528Google Scholar
- Cameron EM (1982) Sulphate and sulphate reduction in early Precambrian oceans. Nature 296:145–148Google Scholar
- Cameron EM (1983) Evidence from early Proterozoic anhydrite for sulfur isotopic partitioning in Precambrian oceans. Nature 304:54–56Google Scholar
- Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396:450–453Google Scholar
- Canfield DE (2004) The evolution of the Earth surface sulfur reservoir. Am J Sci 304(10):839–861Google Scholar
- Canfield DE, Farquhar J (2009) Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proc Acad Sci 106:8123–8127Google Scholar
- Canfield DE, Teske A (1996) Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382:127–132Google Scholar
- Canfield DE, Habicht KS, Thamdrup B (2000) The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288:658–661PubMedGoogle Scholar
- Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315(5808):92–95PubMedGoogle Scholar
- Canil D (2002) Vanadium in peridotites, mantle redox and tectonic environments: Archean to present. Earth Planet Sci Lett 195(1–2):75–90Google Scholar
- Cao CQ, Love GD, Hays LE, Wang W, Shen SZ, Summons RE (2009) Biogeochemical evidence for euxinic oceans and ecological disturbance presaging the end-Permian mass extinction event. Earth Planet Sci Lett 281:188–201Google Scholar
- Carlucci AF, McNally PM (1969) Nitrification by marine bacteria in low concentrations of substrate and oxygen. Limnol Oceanogr 14:736–739Google Scholar
- Carpenter EJ, Romans K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North-Atlantic Ocean. Science 254:1356–1358PubMedGoogle Scholar
- Catling DC (2006) Comment on “A hydrogen-rich early Earth atmosphere”. Science 311(5757):38Google Scholar
- Catling DC, Claire MW (2005) How Earth’s atmosphere evolved to an oxic state: a status report. Earth Planet Sci Lett 237(1–2):1–20Google Scholar
- Catling DC, Zahnle KJ, McKay CP (2001) Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293(5531):839–843PubMedGoogle Scholar
- Catling DC, Zahnle KJ, McKay CP (2002) What caused the second rise of O2 in the late Proterozoic?: methane, sulfate, and irreversible oxidation [Abstract: NASA Astrobiology Institute General Meeting]. Astrobiology 2(4):569Google Scholar
- Chandler FW (1980) Proterozoic redbed sequences of Canada. Can Geol Surv Bull 311:1–53Google Scholar
- Chicarelli MI, Hayes JM, Popp BN, Eckardt CB, Maxwell JR (1993) Carbon and nitrogen isotopic compositions of alkyl porphyrins from the Triassic Serpiano oil-shale. Geochim Cosmochim Acta 57:1307–1311PubMedGoogle Scholar
- Claire MW, Catling DC, Zahnle KJ (2006) Biogeochemical modelling of the rise in atmospheric oxygen. Geobiology 4(4):239–269Google Scholar
- Cloud PE (1973) Paleoecological significance of the banded iron-formation. Econ Geol 68:1135–1143Google Scholar
- Coban-Yildiz Y, Altabet MA, Yilmaz A, Tugrul S (2006) Carbon and nitrogen isotopic ratios of suspended particulate organic matter (SPOM) in the Black Sea water column. Deep-Sea Res II 53:1875–1892Google Scholar
- Coetzee LL (2001) Genetic stratigraphy of the Paleoproterozoic Pretoria Group in the Western Transvaal, MSc. thesis, Rand Afrikaans University, p. 212Google Scholar
- Collier RW (1985) Molybdenum in the Northeast Pacific Ocean. Limnol Oceanogr 30:1351–1354Google Scholar
- Condie KC, Des Marais DJ, Abbott D (2001) Precambrian superplumes and supercontinents: a record in black shales, carbon isotopes, and paleoclimates? Precambr Res 106:239–260Google Scholar
- Czaja AD, Johnson CM, Beard BL, Eigenbrode JL, Freeman KH, Yamaguchi KE (2010) Iron and carbon isotope evidence for ecosystem and environmental diversity in the 2.7 to 2.5 Ga Hamersley Province, Western Australia. Earth Planet Sci Lett 292:170–180Google Scholar
- Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464PubMedGoogle Scholar
- Danielache SO, Eskebjerg C, Johnson MS, Ueno Y, Yoshida N (2008) High-precision spectroscopy of 32S, 33S, and 34S sulfur dioxide: ultraviolet absorption cross sections and isotope effects. J Geophys Res 113:D17314Google Scholar
- Dean DR, Jacobson MR (1992) Biochemical genetics of nitrogenase. In: Stacey G, Burris RH, Evans HJ (eds) Biological Nitrogen Fixation. Chapman and Hall, New York, pp 763–784Google Scholar
- Delano JW (2001) Redox history of the Earth’s interior since similar to 3900 Ma: implications for prebiotic molecules. Origins Life Evol Biosph 31(4–5):311–341Google Scholar
- Delwiche CC, Steyn PL (1970) Nitrogen isotope fractionation in soils and microbial reactions. Environ Sci Technol 4:929–935Google Scholar
- Domagal-Goldman SD, Kasting JF, Johnston DT, Farquhar J (2008) Organic haze, glaciations and multiple sulfur isotopes in the Mid-Archean Era. Earth Planet Sci Lett 269:29–40Google Scholar
- England GL, Rasmussen B, Krapez B, Groves DI (2002) Paleoenvironmental significance of rounded pyrite in siliciclastic sequences of the Late Archean Witwatersrand Basin: oxygen-deficient atmosphere or hydrothermal alteration? Sedimentology 49:1133–1156Google Scholar
- Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels H, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, den Camp H, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548Google Scholar
- Farquhar J, Wing BA (2003) Multiple sulfur isotopes and the evolution of the atmosphere. Earth Planet Sci Lett 213:1–13Google Scholar
- Farquhar J, Bao HM, Thiemens M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289:756–758PubMedGoogle Scholar
- Farquhar J, Savarino J, Airieau S, Thiemens MH (2001) Observation of wavelength-sensitive mass-independent sulfur isotope effects during SO2 photolysis: implications for the early atmosphere. J Geophys Res-Planet 106:32829–32839Google Scholar
- Frank TD, Kah LC, Lyons TW (2003) Changes in organic matter production and accumulation as a mechanism for isotopic evolution in the Mesoproterozoic ocean. Geol Mag 140(4):397–420Google Scholar
- Frei R, Gaucher C, Poulton SW, Canfield DE (2009) Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461:U125–U250Google Scholar
- Fry B, Jannasch HW, Molyneaux SJ, Wirsen CO, Muramoto JA, King S (1991) Stable isotope studies of the carbon, nitrogen and sulfur cycles in the Black-Sea and the Cariaco Trench. Deep-Sea Res A 38:S1003–S1019Google Scholar
- Garvin J, Buick R, Anbar AD, Arnold GL, Kaufman AJ (2009) Isotopic evidence for an aerobic nitrogen cycle in the latest Archean. Science 323:1045–1048PubMedGoogle Scholar
- Gauthier-Lafaye F, Weber F (1989) The Francevillian (Lower Proterozoic) uranium ore deposits of Gabon. Econ Geol 84:2267–2285Google Scholar
- Godfrey LV, Falkowski PG (2009) The cycling and redox state of nitrogen in the Archaean ocean. Nature Geoscience 2:725–729Google Scholar
- Goldblatt C, Lenton TM, Watson AJ (2006) Bistability of atmospheric oxygen and the Great Oxidation. Nature 443(7112):683–686PubMedGoogle Scholar
- Gross GA (1996) Stratiform iron. In: Eckstrand OR, Sinclair WD, Thorpe RI (eds) Canadian mineral deposit types. Geology of Canada. Geological Survey of Canada, Ottawa, pp 41–80Google Scholar
- Grotzinger JP, Kasting JF (1993) New constraints on Precambrian ocean composition. J Geol 101:235–243Google Scholar
- Guo QJ, Strauss H, Kaufman AJ, Schroder S, Gutzmer J, Wing B, Baker MA, Bekker A, Jin QS, Kim ST, Farquhar J (2009) Reconstructing Earth’s surface oxidation across the Archean-Proterozoic transition. Geology 37:399–402Google Scholar
- Habicht KS, Gade M, Thamdrup B, Berg P, Canfield DE (2002) Calibration of sulfate levels in the Archean Ocean. Science 298:2372–2374PubMedGoogle Scholar
- Hannah JL, Bekker A, Stein HJ, Markey RJ, Holland HD (2004) Primitive Os and 2316 Ma age for marine shale: implications for Paleoproterozoic glacial events and the rise of atmospheric oxygen. Earth Planet Sci Lett 225:43–52Google Scholar
- Harrison AG, Thode HG (1958) Mechanism of the bacterial reduction of sulphate from isotope fractionation studies. Trans Faraday Soc 54:84–92Google Scholar
- Hattori K, Campbell FA, Krouse HR (1983a) Sulphur isotope abundances in Aphebian clastic rocks: implications for the coeval atmosphere. Nature 302:323–326Google Scholar
- Hattori K, Krouse HR, Campbell FA (1983b) The start of sulphur oxidation in continental environments: about 2.2 × 109 years ago. Science 221:323–326Google Scholar
- Hattori K, Campbell FA, Krouse HR (1986) Sulphur isotope abundances in sedimentary rocks, relevance to the evolution of the Precambrian atmosphere. Geochem Int 22:97–115Google Scholar
- Hayes JM (1983) Geochemical evidence bearing on the origin of aerobiosis, a seculative hypothesis. In: Schopf JW (ed) The Earth’s Earliest Biosphere: Its Origin and Evolution. Princeton University Press, Princeton, NJ, pp 291–301Google Scholar
- Hayes JM (1994) Global methanotrophy at the Archean-Proterozoic transition. In: Bengston S (ed) Proceedings of nobel symposium 84, Early Life on Earth. Columbia University Press, New York, pp 220–236Google Scholar
- Hayes JM, Waldbauer JR (2006) The carbon cycle and associated redox processes through time. Philos Trans R Soc B 361(1470):931–950Google Scholar
- Heaman LM, Peck D, Toope K (2009) Timing and geochemistry of 1.88 Ga Molson Igneous Events, Manitoba: insights into the formation of a craton-scale magmatic and metallogenic province. Precambr Res 172:143–162Google Scholar
- Helz GR, Miller CV, Charnock JM, Mosselmans JFW, Pattrick RAD, Garner CD, Vaughan DJ (1996) Mechanism of molybdenum removal from the sea and its concentration in black shales: EXAFS evidence. Geochim Cosmochim Acta 60:3631–3642Google Scholar
- Hinrichs KU (2002) Microbial fixation of methane carbon at 2.7 Ga: was an anaerobic mechanism possible? Geochem Geophys Geosyst 3:10Google Scholar
- Hofmann A, Bekker A, Rouxel OJ, Rumble D, Master S (2009) Multiple sulphur and iron isotope composition of detrital pyrite in Archaean sedimentary rocks: a new tool for provenance analysis. Earth Planet Sci Lett 286:436–445Google Scholar
- Holland HD (1973) The oceans: a possible source of iron in iron-formations. Econ Geol Bull Soc Econ Geol 68:1169–1172Google Scholar
- Holland HD (1984) The chemical evolution of the atmosphere and oceans. Princeton University Press, PrincetonGoogle Scholar
- Holland HD (2002) Volcanic gases, black smokers, and the Great Oxidation Event. Geochim Cosmochim Acta 66:3811–3826Google Scholar
- Holland HD (2003) Discussion of the article by A. C. Lasaga and H. Ohmoto on “The oxygen geochemical cycle: dynamics and stability,” Geochim. Cosmochim. Acta 66, 361–381, 2002. Geochim Cosmochim Acta 67:787–789Google Scholar
- Holland HD (2004) The geological history of seawater. In: Holland HD, Turekian KK (eds) Treatise on geochemistry. Elsevier, Oxford, pp 583–625Google Scholar
- Holland HD (2005) Sedimentary mineral deposits and evolution of Earth’s near surface environments. Econ Geol 100:1489–1509Google Scholar
- Holland HD (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc B 361:903–915Google Scholar
- Holland HD (2009) Why the atmosphere became oxygenated: a proposal. Geochim Cosmochim Acta 73:5241–5255Google Scholar
- Isley AE (1995) Hydrothermal plumes and the delivery of iron to banded iron-formation. J Geol 103:169–185Google Scholar
- Isley AE, Abbott DH (1999) Plume-related mafic volcanism and the deposition of banded iron formation. J Geophys Res Solid Earth 104:15461–15477Google Scholar
- Jia YF (2006) Nitrogen isotope fractionations during progressive metamorphism: a case study from the Paleozoic Cooma metasedimentary complex, southeastern Australia. Geochim Cosmochim Acta 70:5201–5214Google Scholar
- Jia YF, Kerrich R (2004) Nitrogen 15-enriched Precambrian kerogen and hydrothermal systems. Geochem Geophys Geosyst 5:Q07005Google Scholar
- Jiang S-Y, Chen Y-Q, Ling H-F, Yang J-H, Feng H-Z, Ni P (2006) Trace- and rare-earth element geochemistry and Pb-Pb dating of black shales and intercalated Ni-Mo-PGE-Au sulfide ores in Lower Cambrian strata, Yangtze Platform, South China. Miner Depos 41:453–467Google Scholar
- Joachimski MM, Ostertag-Hennig C, Pancost RD, Strauss H, Freeman KH, Littke R, Sinninghe Damste JS, Racki G (2001) Water column anoxia, enhanced productivity and concomitant changes in δ13C and δ 34S across the Frasnian-Famennian boundary (Kowala-Holy Cross Mountains/Poland). Chem Geol 175:109–131Google Scholar
- Johnson CM, Beard BL, Roden EE (2008) The iron isotope fingerprints of redox and biogeochemical cycling in the modern and ancient. Earth Ann Rev Earth Planet Sci. 36:457–493Google Scholar
- Johnston DT, Wing BA, Farquhar J, Kaufman AJ, Strauss H, Lyons TW, Kah LC, Canfield DE (2005) Active microbial sulfur disproportionation in the Mesoproterozoic. Science 310(5753):1477–1479PubMedGoogle Scholar
- Junium CK, Arthur MA (2007) Nitrogen cycling during the cretaceous, Cenomanian-Turonian oceanic anoxic event II. Geochem Geophys Geosyst 8:Q03002Google Scholar
- Kah LC, Lyons TW, Frank TD (2004) Low marine sulphate and protracted oxygenation of the proterozoic biosphere. Nature 431(7010):834–838PubMedGoogle Scholar
- Karhu JA, Holland HD (1996) Carbon isotopes and the rise of atmospheric oxygen. Geology 24:867–870Google Scholar
- Kashiyama Y, Ogawa NO, Kuroda J, Shiro M, Nomoto S, Tada R, Kitazato H, Ohkouchi N (2008) Diazotrophic cyanobacteria as the major photoautotrophs during mid-Cretaceous oceanic anoxic events: nitrogen and carbon isotopic evidence from sedimentary porphyrin. Org Geochem 39:532–549Google Scholar
- Kasting JF (1993) Earths early atmosphere. Science 259(5097):920–926PubMedGoogle Scholar
- Kasting JF (2001) Earth history—the rise of atmospheric oxygen. Science 293:819–820PubMedGoogle Scholar
- Kasting JF, Siefert JL (2001) The nitrogen fix. Nature 412:26–27PubMedGoogle Scholar
- Kaufman AJ, Knoll AH (1995) Neoproterozoic variations in the C-isotopic composition of seawater—stratigraphic and biogeochemical implications. Precambrian Res 73:27–49Google Scholar
- Kaufman AJ, Johnston DT, Farquhar J, Masterson AL, Lyons TW, Bates S, Anbar AD, Arnold GL, Garvin J, Buick R (2007) Late Archean biospheric oxygenation and atmospheric evolution. Science 317:1900–1903PubMedGoogle Scholar
- Kendall B, Reinhard CT, Lyons TW, Kaufman AJ, Poulton SW, Anbar AD (2010) Pervasive oxygenation along late Archaean ocean margins: Nat Geosci 3:647–652Google Scholar
- Kirkham RV, Roscoe SM (1993) Atmospheric evolution and ore deposit formation. Resource Geology Special Issue 15:1–17Google Scholar
- Kirschvink JL, Kopp RE (2008) Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II. Philos Trans R Soc B 363(1504):2755–2765Google Scholar
- Konhauser KO, Newman DK, Kappler A (2005) The potential significance of microbial Fe(III) reduction during deposition of Precambrian banded iron formations. Geobiology 3:167–177Google Scholar
- Konhauser KO, Pecoits E, Lalonde SV, Papineau D, Nisbet EG, Barley ME, Arndt NT, Zahnle K, Kamber BS (2009) Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458:750–U785PubMedGoogle Scholar
- Kopp RE, Kirschvink JL, Hilburn IA, Nash CZ (2005) The paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci USA 102(32):11131–11136PubMedGoogle Scholar
- Kulikov YN, Lammer H, Lichtenegger HIM, Penz T, Breuer D, Spohn T, Lundin R, Biernat HK (2007) A comparative study of the influence of the active young sun on the early atmospheres of earth, venus, and mars. Space Sci Rev 129(1–3):207–243Google Scholar
- Kump LR, Barley ME (2007) Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448:1033–1036Google Scholar
- Kump LR, Brantley SL, Arthur MA (2000) Chemical, weathering, atmospheric CO2, and climate. Annu Rev Earth Planet Sci 28:611–667Google Scholar
- Kuypers MMM, van Breugel Y, Schouten S, Erba E, Sinninghe Damste JS (2004) N2-fixing cyanobacteria supplied nutrient N for Cretaceous oceanic anoxic events. Geology 32:853–856Google Scholar
- Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Dimitri G, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106:4752–4757PubMedGoogle Scholar
- Lasaga AC, Otake T, Watanabe Y, Ohmoto H (2008) Anomalous fractionation of sulfur isotopes during heterogeneous reactions. Earth Planet Sci Lett 268:225–238Google Scholar
- Lecuyer C, Ricard Y (1999) Long-term fluxes and budget of ferric iron: implication for the redox states of the Earth’s mantle and atmosphere. Earth Planet Sci Lett 165:197–211Google Scholar
- Li ZXA, Lee CTA (2004) The constancy of upper mantle fO(2) through time inferred from V/Sc ratios in basalts. Earth Planet Sci Lett 228(3–4):483–493Google Scholar
- Lindstrom ES, Tove SR, Wilson PW (1950) Nitrogen fixation by the green and purple sulfur bacteria. Science 112:197–198PubMedGoogle Scholar
- Logan GA, Hayes JM, Hieshima GB, Summons RE (1995) Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376:53–56Google Scholar
- Lyons TW, Werne JP, Hollander DJ, Murray RW (2003) Contrasting sulfur geochemistry and Fe/Al and Mo/Al ratios across the last oxic-to-anoxic transition in the Cariaco Basin, Venezuela. Chem Geol 195:131–157Google Scholar
- MacGregor AM (1927) The problem of the Precambrian atmosphere. S Afr J Sci 24:155–172Google Scholar
- McManus J, Nägler TF, Siebert C, Wheat CG, Hammond DE (2002) Oceanic molybdenum isotope fractionation: diagenesis and hydrothermal ridge-flank alteration. Geochem Geophys Geosys 3:9Google Scholar
- McManus J, Berelson WM, Severmann S, Poulson RL, Hammond DE, Klinkhammer GP, Holm C (2006) Molybdenum and uranium geochemistry in continental margin sediments: paleoproxy potential. Geochim Cosmochim Acta 70:4643–4662Google Scholar
- Melezhik VA, Fallick AE, Medvedev PV, Makarikhin VV (1999) Extreme 13C(carb) enrichment in ca, 2.0 Ga magnesite-stromatolite-dolomite- ‘red beds’ association in a global context: a case for the world-wide signal enhanced by a local environment. Earth Sci Rev 48:71–120Google Scholar
- Melezhik VA, Fallick AE, Hanski EJ, Kump LR, Lepland A, Prave AR, Strauss H (2005) Emergence of the aerobic biosphere during the Archean-Proterozoic transition: challenges of future research today. GSA Today 15:4–11Google Scholar
- Miyake Y, Wada E (1971) The isotope effect on the nitrogen in biochemical, oxidation-reduction reactions. Recent Oceanogr Works Jpn 11:1–6Google Scholar
- Monster J, Appel PWU, Thode HG, Schidlowski M, Carmichael CM, Bridgwater D (1979) Sulfur isotope studies in early Archaean sediments from Isua, West Greenland—implications for the antiquity of bacterial sulfate reduction. Geochim Cosmochim Acta 43:405–413Google Scholar
- Morford JL, Emerson SS (1999) The geochemistry of redox sensitive trace metals in sediments. Geochim Cosmochim Acta 63:1735–1750Google Scholar
- Navarro-Gonzalez R, McKay CP, Mvondo DN (2001) A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412:61–64PubMedGoogle Scholar
- Ohkouchi N, Nakajima Y, Okada H, Ogawa NO, Suga H, Oguri K, Kitazato H (2005) Biogeochemical processes in the saline meromictic Lake Kaiike, Japan: implications from molecular isotopic evidences of photosynthetic pigments. Environ Microbiol 7:1009–1016PubMedGoogle Scholar
- Ohkouchi N, Kashiyama Y, Kuroda J, Ogawa NO, Kitazato H (2006) The importance of diazotrophic cyanobacteria as primary producers during Cretaceous Oceanic Anoxic Event 2. Biogeosciences 3:467–478Google Scholar
- Ono S, Eigenbrode JL, Pavlov AA, Kharecha P, Rumble D, Kasting JF, Freeman KH (2003) New insights into Archean sulfur cycle from mass-independent sulfur isotope records from the Hamersley Basin, Australia. Earth Planet Sci Lett 213:15–30Google Scholar
- Ono S, Beukes NJ, Rumble DI (2009a) Origin of two distinct multiple-sulfur isotope compositions of pyrite in the 2.5 Ga Klein Naute Formation, Griqualand West Basin, South Africa. Precambr Res 169:48–57Google Scholar
- Ono S, Kaufman AJ, Farquhar J, Sumner DY, Beukes NJ (2009b) Lithofacies control on multiple-sulfur isotope records and Neoarchean sulfur cycles. Precambr Res 169:58–67Google Scholar
- Panahi A, Young GM, Rainbird RH (2000) Behaviour of major and trace elements (including REE) during the Paleoproterozoic pedogenesis and diagenetic alteration of an Archean granite near Ville Marie, Quebec, Canada. Geochim Cosmochim Acta 64:2199–2220Google Scholar
- Pancost RD, Crawford N, Magness S, Turner A, Jenkyns H, Maxwell JR (2004) Further evidence for the development of photic-zone euxinic conditions during Mesozoic oceanic anoxic events. Geol Soc (Lond) J 161:353–364Google Scholar
- Papineau D, Mojzsis SJ, Karhu JA, Marty B (2005) Nitrogen isotopic composition of ammoniated phyllosilicates: case studies from Precambrian metamorphosed sedimentary rocks. Chem Geol 216:37–58Google Scholar
- Papineau D, Mojzsis SJ, Schmitt AK (2007) Multiple sulfur isotopes from Paleoproterozoic Huronian interglacial sediments and the rise of atmospheric oxygen. Earth Planet Sci Lett 255:188–212Google Scholar
- Papineau D, Purohit R, Goldberg T, Pi DH, Shields GA, Bhu H, Steele A, Fogel ML (2009) High primary productivity and nitrogen cycling after the Paleoproterozoic phosphogenic event in the Aravalli Supergroup, India. Precambr Res 171:37–56Google Scholar
- Partin C, Bekker A, Scott C, Gill B, Lyons T (2010) Uranium in shales as a proxy for the evolution of surficial redox conditions. GeoCanada 2010: AbstractGoogle Scholar
- Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41PubMedGoogle Scholar
- Pavlov AA, Kasting JF, Eigenbrode JL, Freeman KH (2001) Organic haze in Earth’s early atmosphere: Source of low-C-13 Late Archean kerogens? Geology 29:1003–1006Google Scholar
- Perry EC, Monster J, Reimer TO (1971) Sulfur isotopes in Swaziland System barite and the evolution of Earth’s atmosphere. Science 171:1015–1016PubMedGoogle Scholar
- Peter JM, Goodfellow WD, Doherty W (2003) Hydrothermal sedimentary rocks of the Heath Steele Belt, Bathurst Mining Camp, New Brunswick: part 2, bulk and rare earth element geochemistry and implications for origin. Econ Geol Monogr 11:391–415Google Scholar
- Peters KE, Sweeney RE, Kaplan IR (1978) Correlation of carbon and nitrogen stable isotope ratios in sedimentary organic matter. Limnol Oceanogr 23:598–604Google Scholar
- Pinti DL, Hashizume K (2001) 15N-depleted nitrogen in Early Archean kerogens: clues on ancient marine chemosynthetic-based ecosystems? A comment to Beaumont, V., Robert, F., 1999. Precambrian Res. 96, 62–82. Precambrian Research 105:85–88Google Scholar
- Pinti DL, Hashizume K, Sugihara A, Massault M, Philippot P (2009) Isotopic fractionation of nitrogen and carbon in Paleoarchean cherts from Pilbara craton, Western Australia: Origin of N-15-depleted nitrogen. Geochim Cosmochim Acta 73:3819–3848Google Scholar
- Planavsky N, Rouxel OJ, Bekker A, Shapiro R, Fralick PW, Knudsen A (2009) Iron-oxidizing microbial ecosystems thrived in late Paleoproterozoic redox-stratified oceans. Earth Planet Sci Lett 286:230–242Google Scholar
- Pope MC, Grotzinger JP (2003) Paleoproterozoic stark formation, Athapuscow Basin, Northwest Canada: record of cratonic-scale salinity crisis. J Sediment Res 73:280–295Google Scholar
- Poulton SW, Raiswell R (2002) The low-temperature geochemical cycle of iron: from continental fluxes to marine sediment deposition. Am J Sci 302:774–805Google Scholar
- Poulton SW, Krom MD, Raiswell R (2004) A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide. Geochim Cosmochim Acta 68:3703–3715Google Scholar
- Poulton SW, Bekker A, Canfield DE (2009) Early Paleoproterozoic fluctuations in biospheric oxygenation. Geochim Cosmochim Acta 73:A1047–A1047Google Scholar
- Prasad N, Roscoe SM (1996) Evidence of anoxic to oxic atmosphere change during 2.45–2.22 Ga from lower and upper sub-Huronian paleosols, Canada. Catena 27:105–121Google Scholar
- Rainbird RH, Nesbitt HW, Donaldson JA (1990) Formation and diagenesis of a sub-Huronian saprolith: comparison with a modern weathering profile. J Geol 98:801–822Google Scholar
- Rasmussen B, Buick R (1999) Redox state of the Archean atmosphere: evidence from detrital heavy minerals in ca. 3250–2750 Ma sandstones from the Pilbara Craton, Australia. Geology 27:115–118Google Scholar
- Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101–1104Google Scholar
- Rees CE (1973) Steady-state model for sulfur isotope fractionation in bacterial reduction processes. Geochim Cosmochim Acta 37:1141–1162Google Scholar
- Reinhard CT, Raiswell R, Scott C, Anbar AD, Lyons TW (2009) A late Archean sulfidic sea stimulated by early oxidative weathering of the continents. Science 326:713–716PubMedGoogle Scholar
- Roscoe SM (1996) Paleoplacer uranium gold. In: Eckstrand OR, Sinclair WD, Thorpe RI (eds) Geology of Canadian mineral deposit types, vol P-1. Geological Society of America, The Geology of North America, Boulder, pp 10–23Google Scholar
- Rouxel OJ, Bekker A, Edwards KJ (2005) Iron isotope constraints on the Archean and Paleoproterozoic ocean redox state. Science 307:1088–1091PubMedGoogle Scholar
- Rye R, Holland HD (1998) Paleosols and the evolution of atmospheric oxygen: a critical review. Am J Sci 298:621–672PubMedGoogle Scholar
- Sachs JP, Repeta DJ (1999) Oligotrophy and nitrogen fixation during eastern Mediterranean sapropel events. Science 286:2485–2488PubMedGoogle Scholar
- Sachs JP, Repeta DJ, Goericke R (1999) Nitrogen and carbon isotopic ratios of chlorophyll from marine phytoplankton. Geochim Cosmochim Acta 63:1431–1441Google Scholar
- Schidlowski M (1966) Beiträge zur Kenntnis der radioactiven Bestandteile der Witwatersrand-Konglomerate. I Uranpecherz in den Konglomeraten des Oranje-Freistaat-Goldfeldes. Neues Jahrbuch für Mineralogie Abhandlungen 105:183–202Google Scholar
- Schröder S, Bekker A, Beukes NJ, Strauss H, van Niekerk HS (2008) Rise in seawater sulphate concentration associated with the Paleoproterozoic positive carbon isotope excursion: evidence from sulphate evaporites in the 2.2–2.1 Gyr shallow-marine Lucknow Formation, South Africa. Terra Nova 20:108–117Google Scholar
- Schrum HN, Spivack AJ, Kastner M, D’Hondt S (2009) Sulfate-reducing ammonium oxidation: a thermodynamically feasible metabolic pathway in subseafloor sediment. Geology 37:939–942Google Scholar
- Scott C, Lyons TW, Bekker A, Shen Y, Poulton SW, Chu X, Anbar A (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456–460PubMedGoogle Scholar
- Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK (2009) The continuing puzzle of the Great Oxidation Event. Curr Biol 19:R567–R574PubMedGoogle Scholar
- Shen Y, Farquhar J, Masterson AM, Kaufman AJ, Buick R (2009) Evaluating the role of microbial sulfate reduction in the early Archean using quadruple isotope systematics. Earth Planet Sci Lett 279:383–391Google Scholar
- Sinninghe Damste JS, Koester J (1998) A euxinic southern North Atlantic Ocean during the Cenomanian Turonian oceanic anoxic event. Earth Planet Sci Lett 158:165–173Google Scholar
- Slack JF, Cannon WF (2009) Extraterrestrial demise of banded iron formations 1.85 billion years ago. Geology 37:1011–1014Google Scholar
- Slack JF, Grenne T, Bekker A, Rouxel OJ, Lindberg PA (2007) Suboxic deep seawater in the late Paleoproterozoic: evidence from hematitic chert and iron formation related to seafloor-hydrothermal sulfide deposits, central Arizona, USA. Earth Planet Sci Lett 255:243–256Google Scholar
- Sleep NH, Bird DK (2008) Evolutionary ecology during the rise of dioxygen in the Earth’s atmosphere. Philos Trans R Soc B 363(1504):2651–2664Google Scholar
- Sweeney RE, Liu KK, Kaplan IR (1978) Oceanic nitrogen isotopes and their uses in determining the source of sedimentary nitrogen. In: Robinson BW (ed) Stable Isotopes in the Earth Sciences, vol 220. DSIR Bulletin, Wellington, pp 9–26Google Scholar
- Taylor SR, McLennan SM (1995) The geochemical evolution of the continental crust. Reviews in Geophysics 33:241–265Google Scholar
- Thode HG, Macnamara J, Collins CB (1949) Natural variations in the isotopic content of sulphur and their significance. Can J Res B 27:361–373Google Scholar
- Tian F, Toon OB, Pavlov AA, De Sterck H (2005) A hydrogen-rich early Earth atmosphere. Science 308(5724):1014–1017PubMedGoogle Scholar
- Tian F, Solomon SC, Qian LY, Lei JH, Roble RG (2008) Hydrodynamic planetary thermosphere model: 2. Coupling of an electron transport/energy deposition model. J Geophys Res-Planet 113(E7)Google Scholar
- Tsikos H, Moore JM (1997) Petrography and geochemistry of the Paleoproterozoic Hotazel Iron-Formation, Kalahari Manganese Field, South Africa: Implications for Precambrian Manganes Metallogenesis. Econ Geol 92:87–97Google Scholar
- Turro NJ (1983) Influence of nuclear-spin on chemical-reactions—magnetic isotope and magnetic-field effects (a review). Proc Natl Acad Sci USA 80:609–621PubMedGoogle Scholar
- Ueno Y, Johnson MS, Danielache SO, Eskebjerg C, Pandey A, Yoshida N (2009) Geological sulfur isotopes indicate elevated OCS in the Archean atmosphere, solving faint young sun paradox. Proc Natl Acad Sci USA 106:14784–14789Google Scholar
- Voss M, Nausch G, Montoya JP (1997) Nitrogen stable isotope dynamics in the central Baltic Sea: influence of deep-water renewal on the N-cycle changes. Mar Ecol Prog Ser 158:11–21Google Scholar
- Wahlund TM, Madigan MT (1993) Nitrogen-fixation by the thermophilic green sulfur bacterium Chlorobium tepidum. J Bacteriol 175:81–90Google Scholar
- Watanabe Y, Farquhar J, Ohmoto H (2009) Anomalous fractionations of sulfur isotopes during thermochemical sulfate reduction. Science 324:370–373PubMedGoogle Scholar
- Wellman RP, Cook FD, Krouse HR (1968) Nitrogen-15: microbiological alteration of abundance. Science 161:269–270PubMedGoogle Scholar
- Wille M, Kramers JD, Nagler TF, Beukes NJ, Schroder S, Meisel T, Lacassie JP, Voegelin AR (2007) Evidence for a gradual rise of oxygen between 2.6 and 2.5 Ga from Mo isotopes and Re-PGE signatures in shales. Geochim Cosmochim Acta 71:2417–2435Google Scholar
- Wood J (1973) Stratigraphy and depositional environments of upper Huronian rocks of the Rawhide Lake-Flack Lake area, Ontario. In: Young GM (ed) Huronian Stratigraphy and Sedimentation, vol 12. Geological Association of Canada Special Paper, Geological Association of Canada, pp 73–95Google Scholar
- Yamaguchi KE (2002) Geochemistry of Archean-Paleoproterozoic black shales: early evolution of the atmosphere, oceans, and biosphere, Ph.D. dissertation, Department of Geosciences, Pennsylvania State University, 456 ppGoogle Scholar
- Yamaguchi KE, Ohmoto H (2006) Comment on “Iron isotope constraints on the Archean and Paleoproterozoic ocean redox state”. Science 311:177aGoogle Scholar
- Yamaguchi KE, Johnson CM, Beard BL, Ohmoto H (2005) Biogeochemical cycling of iron in the Archean-Paleoproterozoic Earth: constraints from iron isotope variations in sedimentary rocks from the Kaapvaal and Pilbara Cratons. Chem Geol 218:135–169Google Scholar
- Yang W, Holland HD (2002) The redox-sensitive trace elements, Mo, U, and Re in Precambrian carbonaceous shales: indicators of the Great Oxidation Event. GSA Abstr Progr 34:381Google Scholar
- Yang W, Holland HD (2003) The Hekpoort paleosol profile in Strata 1 at Gaborone, Botswana: soil formation during the great oxidation event. Am J Sci 303:187–220Google Scholar
- Zahnle K, Claire M, Catling D (2006) The loss of mass-independent fractionation in sulfur due to a Palaeoproterozoic collapse of atmospheric methane. Geobiology 4(4):271–283Google Scholar
- Zerkle AL, Junium CK, Canfield DE, House CH (2008) Production of 15N-depleted biomass during cyanobacterial N2-fixation at high Fe concentrations. J Geophys Res 113:G03014Google Scholar