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Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity

Naturevolume 559pages613616 (2018) | Download Citation


The global biosphere is commonly assumed to have been less productive before the rise of complex eukaryotic ecosystems than it is today1. However, direct evidence for this assertion is lacking. Here we present triple oxygen isotope measurements (∆17O) from sedimentary sulfates from the Sibley basin (Ontario, Canada) dated to about 1.4 billion years ago, which provide evidence for a less productive biosphere in the middle of the Proterozoic eon. We report what are, to our knowledge, the most-negative ∆17O values (down to −0.88‰) observed in sulfates, except for those from the terminal Cryogenian period2. This observation demonstrates that the mid-Proterozoic atmosphere was distinct from what persisted over approximately the past 0.5 billion years, directly reflecting a unique interplay among the atmospheric partial pressures of CO2 and O2 and the photosynthetic O2 flux at this time3. Oxygenic gross primary productivity is stoichiometrically related to the photosynthetic O2 flux to the atmosphere. Under current estimates of mid-Proterozoic atmospheric partial pressure of CO2 (2–30 times that of pre-anthropogenic levels), our modelling indicates that gross primary productivity was between about 6% and 41% of pre-anthropogenic levels if atmospheric O2 was between 0.1–1% or 1–10% of pre-anthropogenic levels, respectively. When compared to estimates of Archaean4,5,6 and Phanerozoic primary production7, these model solutions show that an increasingly more productive biosphere accompanied the broad secular pattern of increasing atmospheric O2 over geologic time8.

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  1. 1.

    Anbar, A. D. & Knoll, A. H. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137–1142 (2002).

  2. 2.

    Bao, H., Lyons, J. R. & Zhou, C. Triple oxygen isotope evidence for elevated CO2 levels after a Neoproterozoic glaciation. Nature 453, 504–506 (2008).

  3. 3.

    Cao, X. & Bao, H. Dynamic model constraints on oxygen-17 depletion in atmospheric O2 after a snowball Earth. Proc. Natl Acad. Sci. USA 110, 14546–14550 (2013).

  4. 4.

    Kharecha, P., Kasting, J. & Siefert, J. A coupled atmosphere–ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005).

  5. 5.

    Canfield, D. E., Rosing, M. T. & Bjerrum, C. Early anaerobic metabolisms. Phil. Trans. R. Soc. Lond. B 361, 1819–1836 (2006).

  6. 6.

    Ward, L. M., Kirschvink, J. L. & Fischer, W. W. Timescales of oxygenation following the evolution of oxygenic photosynthesis. Orig. Life Evol. Biosph. 46, 51–65 (2016).

  7. 7.

    Wing, B. A. A cold, hard look at ancient oxygen. Proc. Natl Acad. Sci. USA 110, 14514–14515 (2013).

  8. 8.

    Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).

  9. 9.

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

  10. 10.

    Sánchez-Baracaldo, P., Ridgwell, A. & Raven, J. A. A Neoproterozoic transition in the marine nitrogen cycle. Curr. Biol. 24, 652–657 (2014).

  11. 11.

    Derry, L. A. Causes and consequences of mid-Proterozoic anoxia. Geophys. Res. Lett. 42, 8538–8546 (2015).

  12. 12.

    Reinhard, C. T. et al. Evolution of the global phosphorus cycle. Nature 541, 386–389 (2017).

  13. 13.

    Koehler, M. C. et al. Spatial and temporal trends in Precambrian nitrogen cycling: a Mesoproterozoic offshore nitrate minimum. Geochim. Cosmochim. Acta 198, 315–337 (2017).

  14. 14.

    Buick, R., Des Marais, D. J. & Knoll, A. H. Stable isotopic compositions of carbonates from the Mesoproterozoic Bangemall Group, northwestern Australia. Chem. Geol. 123, 153–171 (1995).

  15. 15.

    Wen, J. & Thiemens, M. H. Multi-isotope study of the O (1 D)+ CO2 exchange and stratospheric consequences. J. Geophys. Res. 98, 12801–12808 (1993).

  16. 16.

    Yung, Y. L., DeMore, W. B. & Pinto, J. P. Isotopic exchange between carbon dioxide and ozone via O(1D) in the stratosphere. Geophys. Res. Lett. 18, 13–16 (1991).

  17. 17.

    Luz, B., Barkan, E., Bender, M. L., Thiemens, M. H. & Boering, K. A. Triple-isotope composition of atmospheric oxygen as a tracer of biosphere productivity. Nature 400, 547–550 (1999).

  18. 18.

    Bender, M., Sowers, T. & Labeyrie, L. The Dole effect and its variations during the last 130,000 years as measured in the Vostok ice core. Glob. Biogeochem. Cycles 8, 363–376 (1994).

  19. 19.

    Segura, A. et al. Ozone concentrations and ultraviolet fluxes on Earth-like planets around other stars. Astrobiology 3, 689–708 (2003).

  20. 20.

    Bao, H., Rumble, D. III & Lowe, D. R. The five stable isotope compositions of Fig Tree barites: implications on sulfur cycle in ca. 3.2 Ga oceans. Geochim. Cosmochim. Acta 71, 4868–4879 (2007).

  21. 21.

    Percak-Dennett, E. et al. Microbial acceleration of aerobic pyrite oxidation at circumneutral pH. Geobiology 15, 690–703 (2017).

  22. 22.

    Balci, N., Shanks, W. C. III, Mayer, B. & Mandernack, K. W. Oxygen and sulfur isotope systematics of sulfate produced by bacterial and abiotic oxidation of pyrite. Geochim. Cosmochim. Acta 71, 3796–3811 (2007).

  23. 23.

    Antler, G., Turchyn, A. V., Rennie, V., Herut, B. & Sivan, O. Coupled sulfur and oxygen isotope insight into bacterial sulfate reduction in the natural environment. Geochim. Cosmochim. Acta 118, 98–117 (2013).

  24. 24.

    Pellerin, A. et al. Mass-dependent sulfur isotope fractionation during reoxidative sulfur cycling: a case study from Mangrove Lake, Bermuda. Geochim. Cosmochim. Acta 149, 152–164 (2015).

  25. 25.

    Pack, A. et al. Tracing the oxygen isotope composition of the upper Earth's atmosphere using cosmic spherules. Nat. Comm. 8, 15702 (2017).

  26. 26.

    Hardie, L. A. The origin of the recent non-marine evaporite deposit of Saline Valley, Inyo County, California. Geochim. Cosmochim. Acta 32, 1279–1301 (1968).

  27. 27.

    Ryu, J.-H., Zierenberg, R. A., Dahlgren, R. A. & Gao, S. Sulfur biogeochemistry and isotopic fractionation in shallow groundwater and sediments of Owens Dry Lake, California. Chem. Geol. 229, 257–272 (2006).

  28. 28.

    Rogala, B., Fralick, P. W., Heaman, L. M. & Metsaranta, R. Lithostratigraphy and chemostratigraphy of the Mesoproterozoic Sibley Group, northwestern Ontario, Canada. Can. J. Earth Sci. 44, 1131–1149 (2007).

  29. 29.

    Bao, H., Fairchild, I. J., Wynn, P. M. & Spötl, C. Stretching the envelope of past surface environments: Neoproterozoic glacial lakes from Svalbard. Science 323, 119–122 (2009).

  30. 30.

    Johnston, D. T. et al. Active microbial sulfur disproportionation in the Mesoproterozoic. Science 310, 1477–1479 (2005).

  31. 31.

    Kunzmann, M. et al. Zn isotope evidence for immediate resumption of primary productivity after snowball Earth. Geology 41, 27–30 (2013).

  32. 32.

    Brocks, J. J. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017).

  33. 33.

    Ward, B. A., Dutkiewicz, S. & Follows, M. J. Modelling spatial and temporal patterns in size-structured marine plankton communities: top–down and bottom–up controls. J. Plankton Res. 36, 31–47 (2013).

  34. 34.

    Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

  35. 35.

    Eppley, R. W. & Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677–680 (1979).

  36. 36.

    Close, H. G. et al. Export of submicron particulate organic matter to mesopelagic depth in an oligotrophic gyre. Proc. Natl Acad. Sci. USA 110, 12565–12570 (2013).

  37. 37.

    Logan, G. A., Hayes, J. M., Hieshima, G. B. & Summons, R. E. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376, 53–56 (1995).

  38. 38.

    Close, H. G., Bovee, R. & Pearson, A. Inverse carbon isotope patterns of lipids and kerogen record heterogeneous primary biomass. Geobiology 9, 250–265 (2011).

  39. 39.

    Peng, Y., Bao, H., Zhou, C. & Yuan, X. 17O-depleted barite from two Marinoan cap dolostone sections, South China. Earth Planet. Sci. Lett. 305, 21–31 (2011).

  40. 40.

    Killingsworth, B. A., Hayles, J. A., Zhou, C. & Bao, H. Sedimentary constraints on the duration of the Marinoan Oxygen-17 Depletion (MOSD) event. Proc. Natl Acad. Sci. USA 110, 17686–17690 (2013).

  41. 41.

    Crockford, P. W. et al. Linking paleocontinents through triple oxygen isotope anomalies. Geology 46, 179–182 (2017).

  42. 42.

    Crockford, P. W. et al. Triple oxygen and multiple sulfur isotope constraints on the evolution of the post-Marinoan sulfur cycle. Earth Planet. Sci. Lett. 435, 74–83 (2016).

  43. 43.

    Bao, H., Chen, Z.-Q. & Zhou, C. An 17O record of late Neoproterozoic glaciation in the Kimberley region, Western Australia. Precambr. Res. 216–219, 152–161 (2012).

  44. 44.

    Cowie, B. R. & Johnston, D. T. High-precision measurement and standard calibration of triple oxygen isotopic compositions (δ18O, Δ′17O) of sulfate by F2 laser fluorination. Chem. Geol. 440, 50–59 (2016).

  45. 45.

    Sim, M. S., Bosak, T. & Ono, S. Large sulfur isotope fractionation does not require disproportionation. Science 333, 74–77 (2011).

  46. 46.

    Davis, D. W. & Sutcliffe, R. H. U–Pb ages from the Nipigon plate and northern Lake Superior. Geol. Soc. Am. Bull. 96, 1572–1579 (1985).

  47. 47.

    Franklin, J. M. in Rubidium–Strontium Isotopic Age Studies, Report 2 (eds Wanless, R. K. & Loveridge, W. D.) 77–14 (Geological Survey of Canada, Ottawa, 1978).

  48. 48.

    Robertson, W. A. Pole position from thermally cleaned Sibley Group sediments and its relevance to Proterozoic magnetic stratigraphy. Can. J. Earth Sci. 10, 180–193 (1973).

  49. 49.

    Elston, D. P., Enkin, R. J., Baker, J. D. & Kisilevsky, K. Tightening the belt: paleomagnetism-stratigraphic constraints on deposition, correlation, and deformation of the Middle Proterozoic (ca. 1.4 Ga) Belt-Purcell Supergroup, United States and Canada. Geol. Soc. Am. Bull. 114, 619–638 (2002).

  50. 50.

    Cheadle, B. A. Alluvial-playa sedimentation in the lower Keweenawan Sibley Group, Thunder Bay District, Ontario. Can. J. Earth Sci. 23, 527–542 (1986).

  51. 51.

    Metsaranta, R. T. Sedimentology and Geochemistry of the Mesoproterozoic Pass Lake and Rossport Formations, Sibley Group. MSc thesis, Lakehead Univ. (2006).

  52. 52.

    Bao, H. Purifying barite for oxygen isotope measurement by dissolution and reprecipitation in a chelating solution. Anal. Chem. 78, 304–309 (2006).

  53. 53.

    Bao, H. & Thiemens, M. H. Generation of O2 from BaSO4 using a CO2-laser fluorination system for simultaneous analysis of δ18O and δ17O. Anal. Chem. 72, 4029–4032 (2000).

  54. 54.

    Matsuhisa, Y., Goldsmith, J. R. & Clayton, R. N. Mechanisms of hydrothermal crystallization of quartz at 250 °C and 15 kbar. Geochim. Cosmochim. Acta 42, 173–182 (1978).

  55. 55.

    Cao, X. & Liu, Y. Equilibrium mass-dependent fractionation relationships for triple oxygen isotopes. Geochim. Cosmochim. Acta 75, 7435–7445 (2011).

  56. 56.

    Bao, H., Cao, X. & Hayles, J. A. Triple oxygen isotopes: fundamental relationships and applications. Annu. Rev. Earth Planet. Sci. 44, 463–492 (2016).

  57. 57.

    Miller, M. F. Isotopic fractionation and the quantification of 17O anomalies in the oxygen three-isotope system: an appraisal and geochemical significance. Geochim. Cosmochim. Acta 66, 1881–1889 (2002).

  58. 58.

    Angert, A., Rachmilevitch, S., Barkan, E. & Luz, B. Effects of photorespiration, the cytochrome pathway, and the alternative pathway on the triple isotopic composition of atmospheric O2. Glob. Biogeochem. Cycles 17, 1030 (2003).

  59. 59.

    Thode, H. G., Monster, J. & Dunford, H. B. Sulphur isotope geochemistry. Geochim. Cosmochim. Acta 25, 159–174 (1961).

  60. 60.

    Shaheen, R., Janssen, C. & Röckmann, T. Investigations of the photochemical isotope equilibrium between O2, CO2 and O3. Atmos. Chem. Phys. 7, 495–509 (2007).

  61. 61.

    von Paris, P. et al. Warming the early Earth—CO2 reconsidered. Planet. Space Sci. 56, 1244–1259 (2008).

  62. 62.

    Wolf, E. T. & Toon, O. B. Controls on the Archean climate system investigated with a global climate model. Astrobiology 14, 241–253 (2014).

  63. 63.

    Mills, B., Lenton, T. M. & Watson, A. J. Proterozoic oxygen rise linked to shifting balance between seafloor and terrestrial weathering. Proc. Natl Acad. Sci. USA 111, 9073–9078 (2014).

  64. 64.

    Kaufman, A. J. & Xiao, S. High CO2 levels in the Proterozoic atmosphere estimated from analyses of individual microfossils. Nature 425, 279–282 (2003).

  65. 65.

    Sheldon, N. D. Causes and consequences of low atmospheric pCO2 in the Late Mesoproterozoic. Chem. Geol. 362, 224–231 (2013).

  66. 66.

    Hansen, J. et al. Target atmospheric CO2: where should humanity aim? Open Atmos. Sci. J. 2, 217–231 (2008).

  67. 67.

    Kasting, J. F. & Donahue, T. M. The evolution of atmospheric ozone. J. Geophys. Res. Oceans 85, 3255–3263 (1980).

  68. 68.

    Pavlov, A. A. & Kasting, J. F. Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27–41 (2002).

  69. 69.

    Horner, T. J. et al. Pelagic barite precipitation at micromolar ambient sulfate. Nat. Commun. 8, 1342 (2017).

  70. 70.

    Holland, H. D., Feakes, C. R. & Zbinden, E. A. The Flin Flon paleosol and the composition of the atmosphere 1.8 BYBP. Am. J. Sci. 289, 362–389 (1989).

  71. 71.

    Planavsky, N. J. et al. Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638 (2014).

  72. 72.

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

  73. 73.

    Gilleaudeau, G. J. et al. Oxygenation of the mid-Proterozoic atmosphere: clues from chromium isotopes in carbonates. Geochem. Perspect. Lett. 2, 178–187 (2016).

  74. 74.

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

  75. 75.

    Planavsky, N. J. et al. No evidence for high atmospheric oxygen levels 1,400 million years ago. Proc. Natl Acad. Sci. USA 113, E2550–E2551 (2016).

  76. 76.

    Liu, X. M. et al. Tracing Earth’s O2 evolution using Zn/Fe ratios in marine carbonates. Geochem. Perspect. Lett. 2, 24–34 (2016).

  77. 77.

    Canfield, D. E. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998).

  78. 78.

    Reinhard, C. T. et al. Proterozoic ocean redox and biogeochemical stasis. Proc. Natl Acad. Sci. USA 110, 5357–5362 (2013).

  79. 79.

    Cox, G. M. et al. Basin redox and primary productivity within the Mesoproterozoic Roper Seaway. Chem. Geol. 440, 101–114 (2016).

  80. 80.

    Daines, S. J., Mills, B. J. & Lenton, T. M. Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon. Nat. Commun. 8, 14379 (2017).

  81. 81.

    Runnegar, B. Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Global Planet. Change 5, 97–111 (1991).

  82. 82.

    Sperling, E. A., Halverson, G. P., Knoll, A. H., Macdonald, F. A. & Johnston, D. T. A basin redox transect at the dawn of animal life. Earth Planet. Sci. Lett. 371–372, 143–155 (2013).

  83. 83.

    Mills, D. B. et al. Oxygen requirements of the earliest animals. Proc. Natl Acad. Sci. USA 111, 4168–4172 (2014).

  84. 84.

    Kohl, I. & Bao, H. Triple-oxygen-isotope determination of molecular oxygen incorporation in sulfate produced during abiotic pyrite oxidation (pH= 2–11). Geochim. Cosmochim. Acta 75, 1785–1798 (2011).

  85. 85.

    Hayles, J. A., Cao, X. & Bao, H. The statistical mechanical basis of the triple isotope fractionation relationship. Geochem. Perspect. Lett. 3, 1–11 (2017).

  86. 86.

    Trenberth, K. & Smith, E. L. The mass of the atmosphere: a constraint on global analyses. J. Clim. 18, 864–875 (2005).

  87. 87.

    Linz, M. et al. The strength of the meridional overturning circulation of the stratosphere. Nat. Geosci. 10, 663–667 (2017).

  88. 88.

    Butchart, N. et al. Simulations of anthropogenic change in the strength of the Brewer–Dobson circulation. Clim. Dyn. 27, 727–741 (2006).

  89. 89.

    Fiorella, R. P. & Sheldon, N. D. Equable end Mesoproterozoic climate in the absence of high CO2. Geology 45, 231–234 (2017).

  90. 90.

    Gibson, T. M. et al. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46, 135–138 (2018).

  91. 91.

    Kah, L. C. & Riding, R. Mesoproterozoic carbon dioxide levels inferred from calcified cyanobacteria. Geology 35, 799–802 (2007).

  92. 92.

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

  93. 93.

    Goldblatt, C., Lenton, T. M. & Watson, A. J. Bistability of atmospheric oxygen and the Great Oxidation. Nature 443, 683–686 (2006).

  94. 94.

    Zhang, S. et al. The oxic degradation of sedimentary organic matter 1400 Ma constrains atmospheric oxygen levels. Biogeosciences 14, 2133–2149 (2017).

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P.W.C. acknowledges funding from a Natural Sciences and Engineering Research Council of Canada (NSERC) PGS-D grant. This research was supported by funding from NSERC, the Fonds de Recherche du Québec–Nature et Technologies, and the University of Colorado Boulder (B.A.W.). H.B. acknowledges funding from the strategic priority research program (B) of CAS (XDB18010104). We thank E. Wolf, N. Cowan, S. Becker, Y. Slichter and L. Derry for discussions on the assumptions, methods and implications of our study.

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Nature thanks B. Passey and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information


  1. McGill University, Montreal, Quebec, Canada

    • Peter W. Crockford
    • , Galen P. Halverson
    •  & Thi Hao Bui
  2. Weizmann Institute of Science, Rehovot, Israel

    • Peter W. Crockford
  3. Princeton University, Princeton, NJ, USA

    • Peter W. Crockford
  4. Rice University, Houston, TX, USA

    • Justin A. Hayles
  5. Louisiana State University, Baton Rouge, LA, USA

    • Justin A. Hayles
    • , Huiming Bao
    •  & Yongbo Peng
  6. School of Earth & Space Sciences, Peking University, Beijing, China

    • Huiming Bao
  7. Yale University, New Haven, CT, USA

    • Noah J. Planavsky
  8. University of California Riverside, Riverside, CA, USA

    • Andrey Bekker
  9. Lakehead University, Thunder Bay, Ontario, Canada

    • Philip W. Fralick
  10. University of Colorado Boulder, Boulder, CO, USA

    • Boswell A. Wing


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P.W.C. and B.A.W. designed research. N.J.P., A.B. and P.W.F. provided samples. P.W.C., J.A.H., Y.P. and T.H.B. performed isotopic analyses. P.W.C. and B.A.W. conducted modelling. P.W.C. wrote the manuscript with contributions from B.A.W., N.J.P. and A.B., and input from all co-authors.

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Extended data figures and tables

  1. Extended Data Fig. 1 Histograms of existing data for ∆17O values through Earth history.

    The histograms show Phanerozoic sulfates2 (n = 51; light grey), syn-Marinoan CAS29 (n = 25; dark grey), post-Marinoan barite2,39,40,41,42 (n = 213; blue) and results from the Sibley sulfates (n = 68; red).

  2. Extended Data Fig. 2 Compiled \({{\boldsymbol{p}}}_{{{\bf{CO}}}_{{\bf{2}}}}\) and \({{\boldsymbol{p}}}_{{{\bf{O}}}_{{\bf{2}}}}\) estimates.

    a, \({p}_{{{\rm{CO}}}_{2}}\) estimates. Left y axis, percentage of PAL; right y axis, p.p.m. Grey band outlines results from 1D modelling61 based on temperatures of 273 K (bottom), 288 K (top) and changing solar luminosity. Red dotted lines represent extrapolated general circulation model (GCM) results62 from Archaean estimates. The green-shaded region represents the uncertainty envelope of palaeosol-based estimates65 with the green dotted lines interpolating between estimates at 1.8 and 1.1 Ga together. The pink-shaded region represents estimates based on the COPSE Earth system model63. The brown bar represents modelling-based estimates required to prevent a global glaciation at 1.1 Ga89. The dark-blue square is the microfossil-based estimate that sets maximum limits at 1.05 Ga90,91. Yellow arrows represent the upper (30 PAL) and lower (2 PAL) limits used in this work. Data are from previous publications61,62,63,65,89,91. b, \({p}_{{{\rm{O}}}_{2}}\) estimates. Green arrows represent biologically based estimates; blue arrows represent geochemical estimates; and in red are modelling \({p}_{{{\rm{O}}}_{2}}\) estimates. Purple lines represent the removal of S-MIF92, a proposed bistability field93, and constraints on the establishment of a modern-like ozone layer13,67. The yellow dashed line represents the suggested limits for the removal of deep ocean anoxia76, and the grey dashed line represents the appearance of charcoal. Data are from previous publications9,19,67,68,70,71,72,74,76,77,80,81,82,83,93,94.

  3. Extended Data Fig. 3 Probability distribution functions for the control parameters of the model.

    The justification for the form (Gaussian or uniform), the spread (standard deviation or range) and the mean of each distribution is given in the main text and Methods.

  4. Extended Data Fig. 4 Realization of about 10,000 Monte Carlo calculations of GPP (PAL) relative to various control parameters in the isotope mass-balance model.

    a, Unlike model calculations for the Neoproterozoic era, there is no clear strong dependence of GPP on assumed \({p}_{{{\rm{CO}}}_{2}}\). b, There is a clear log-linear dependence of the GPP estimates on \({p}_{{{\rm{O}}}_{2}}\). c, GPP responds weakly to \({f}_{{{\rm{O}}}_{2}}\), with large fractions of O2 in sulfate (which indicate smaller ∆17OO2 values) leading to higher estimates of GPP. d, The response of GPP to ∆17Osulfate is similar to the response to \({f}_{{{\rm{O}}}_{2}}\). Smaller ∆17Osulfate values indicate smaller ∆17OO2 values, which—all else being the same—requires greater GPP. e, GPP estimates seem to be largely independent of gamma.

  5. Extended Data Fig. 5 Realization of about 20,000 Monte Carlo calculations of GPP (PAL) and \({{\boldsymbol{p}}}_{{{\bf{O}}}_{{\bf{2}}}}\).

    a, Results are calculated to be consistent with the Δ17O measurements in Extended Data Table 1 and the probability distribution functions shown in Extended Data Fig. 2, with the exception of \({p}_{{{\rm{O}}}_{2}}\). These calculations assume restricted ranges of \({p}_{{{\rm{O}}}_{2}}\) between 0.1% and 1% PAL (orange histogram) and between 1% and 10% PAL (blue histogram). In both cases the bimodality seen in the full suite of Monte Carlo calculations (Fig. 3) disappears, and both sets of calculations are well-approximated by single-peaked Gaussian probability density functions. This confirms that \({p}_{{{\rm{O}}}_{2}}\) is the dominant control on the bimodal structure seen in the full suite of Monte Carlo calculations (Fig. 3), and justifies our division of those results into a pair of Gaussian probability density functions, one associated with \({p}_{{{\rm{O}}}_{2}}\) between 0.1% and 1% PAL and another associated with \({p}_{{{\rm{O}}}_{2}}\) between 1% and 10% PAL. b, Results are solutions that are consistent with the ∆17Osulfate dataset (Extended Data Table 1), the probability density functions shown in Extended Data Fig. 1 (with the exception of \({p}_{{{\rm{O}}}_{2}}\)) and the mean GPP estimates of the two inferred Gaussian probability distributions for mid-Proterozoic GPP (Fig. 3). GPP was allowed to vary in a Gaussian fashion between the 95% confidence limits on the GPP mean values.

  6. Extended Data Fig. 6 Geological map of the Lake Nipigon–northern Lake Superior region.

    This figure was adapted from a previous publication28. © 2008 Canadian Science Publishing or its licensors. Reproduced with permission.

  7. Extended Data Fig. 7 Oxygen and sulfur isotope compositions (∆17O, δ18O, δ34S and ∆33S) for sulfates from drill hole NI-92-7 plotted against stratigraphic height.

    Uncertainty on all analyses is smaller than the sizes of the data points.

  8. Extended Data Table 1 Isotopic data and comparisons with previously published results
  9. Extended Data Table 2 Summary of reference parameters for model calculations

Supplementary information

  1. Supplementary Information

    This file contains Supplementary Text including a discussion of data and model equations.

  2. Reporting Summary

  3. Supplementary Table

    This file contains Supplementary Table 1.

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