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High CO2 levels in the Proterozoic atmosphere estimated from analyses of individual microfossils


Solar luminosity on the early Earth was significantly lower than today. Therefore, solar luminosity models suggest that, in the atmosphere of the early Earth, the concentration of greenhouse gases such as carbon dioxide and methane must have been much higher1,2. However, empirical estimates of Proterozoic levels of atmospheric carbon dioxide concentrations have not hitherto been available. Here we present ion microprobe analyses of the carbon isotopes in individual organic-walled microfossils extracted from a Proterozoic ( 1.4-gigayear-old) shale in North China. Calculated magnitudes of the carbon isotope fractionation in these large, morphologically complex microfossils suggest elevated levels of carbon dioxide in the ancient atmosphere—between 10 and 200 times the present atmospheric level. Our results indicate that carbon dioxide was an important greenhouse gas during periods of lower solar luminosity, probably dominating over methane after the atmosphere and hydrosphere became pervasively oxygenated between 2 and 2.2 gigayears ago.

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Figure 1: Photographs of D. delicata specimens used in this study.
Figure 2: Relationship between carbon isotopic fractionation of the Calvin cycle (ɛp) and CO2 concentration in sea water (Ce) at different growth rates (µ, in units of d-1).
Figure 3: Atmospheric p CO 2 levels in the Archaean and Proterozoic.


  1. Kasting, J. F. Earth's early atmosphere. Science 259, 920–926 (1993)

    ADS  CAS  Article  Google Scholar 

  2. Pavlov, A. A., Hurtgen, M. T., Kasting, J. F. & Arthur, M. A. Methane-rich Proterozoic atmosphere? Geology 31, 87–90 (2003)

    ADS  CAS  Article  Google Scholar 

  3. Xiao, S., Knoll, A. H., Kaufman, A. J., Yin, L. & Zhang, Y. Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform. Precambr. Res. 84, 197–220 (1997)

    ADS  CAS  Article  Google Scholar 

  4. Brasier, M. D. & Lindsay, J. F. A billion years of environmental stability and the emergence of eukaryotes: New data from northern Australia. Geology 26, 555–558 (1998)

    ADS  CAS  Article  Google Scholar 

  5. Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66–69 (2001)

    ADS  CAS  Article  Google Scholar 

  6. Shively, J. M. & Barton, L. L. Variations in Autotrophic Life 1–346 (Academic, New York, 1991)

    Google Scholar 

  7. Schulz, H. et al. Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284, 493–495 (1999)

    ADS  CAS  Article  Google Scholar 

  8. Cristy, S. S. in Inorganic Mass Spectrometry (eds Barshick, C.M., Duckworth, D.C. & Smith, D.H.) 159–221 (Marcel Dekker, New York, 2000)

    Google Scholar 

  9. House, C. H. et al. Carbon isotope composition of individual Precambrian microfossils. Geology 28, 707–710 (2000)

    ADS  CAS  Article  Google Scholar 

  10. Ueno, Y., Isozaki, Y., Yurimoto, H. & Maruyama, S. Carbon isotopic signatures of individual Archean microfossils(?) from Western Australia. Int. Geol. Rev. 43, 196–212 (2001)

    Article  Google Scholar 

  11. Hayes, J. M., Strauss, H. & Kaufman, A. J. The abundance of C-13 in marine organic matter and isotopic fractionation in the global biogeochemical cycle of carbon during the past 800 Ma. Chem. Geol. 16, 103–125 (1999)

    ADS  Article  Google Scholar 

  12. Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C. & Macko, S. A. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2(aq)]: Theoretical considerations and experimental results. Geochim. Cosmochim. Acta 59, 1131–1138 (1995)

    ADS  CAS  Article  Google Scholar 

  13. Laws, E. A., Bidigare, R. R. & Popp, B. N. Effect of growth rate and CO2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol. Oceanogr. 42, 1552–1560 (1997)

    ADS  CAS  Article  Google Scholar 

  14. Popp, B. N. et al. Effect of phytoplankton geometry on carbon isotopic fractionation. Geochim. Cosmochim. Acta 62, 69–77 (1998)

    ADS  CAS  Article  Google Scholar 

  15. Bidigare, R. R. et al. Consistent fractionation of C-13 in nature and in the laboratory: Growth-rate effects in some haptophyte algae. Glob. Geochem. Cycles 13, 251–252 (1999)

    ADS  CAS  Article  Google Scholar 

  16. Knoll, A. H. Microbiotas of the late Precambrian Hunnberg Formation, Nordaustlandet, Svalbard. J. Paleontol. 58, 131–162 (1984)

    Google Scholar 

  17. Grotzinger, J. P. & Kasting, J. F. New constraints on Precambrian ocean composition. J. Geol. 101, 235–243 (1993)

    ADS  CAS  Article  Google Scholar 

  18. Rye, R., Kuo, P. H. & Holland, H. D. Atmospheric carbon-dioxide concentrations before 2.2-billion years ago. Nature 378, 603–605 (1995)

    ADS  CAS  Article  Google Scholar 

  19. Holland, H. D. in Early Life on Earth (ed. Bengtson, S.) 237–244 (Columbia Univ. Press, New York, 1994)

    Google Scholar 

  20. Karhu, J. & Holland, H. Carbon isotopes and the rise of atmospheric oxygen. Geology 24, 867–870 (1996)

    ADS  CAS  Article  Google Scholar 

  21. Habicht, K. S., Gade, M., Thamdrup, B., Berg, P. & Canfield, D. E. Calibration of sulfate levels in the Archean oceans. Science 298, 2372–2374 (2002)

    ADS  CAS  Article  Google Scholar 

  22. Farquhar, J., Hauri, E. & Wang, J. New insights into carbon fluid chemistry and graphite precipitation: SIMS analysis of granulite facies graphite from Ponmudi, South India. Earth Planet. Sci. Lett. 171, 607–621 (1999)

    ADS  CAS  Article  Google Scholar 

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We thank the following for technical assistance; E. Hauri, J. Wang, J. Orloff, R. Dotson, K. Livi, D. Veblen and P. Piccoli. We also thank A. Knoll and L. Yin for providing samples for bulk rock analyses, and J. Hayes for comments on an earlier version of this manuscript. This research was supported by NASA Exobiology, NSF Geology and Paleontology, and China MOST 973 programs.

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Correspondence to Alan J. Kaufman or Shuhai Xiao.

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

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