Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Early oxygenation of the terrestrial environment during the Mesoproterozoic

Nature volume 468, pages 290–293 (2010)Cite this article

Subjects

Abstract

Geochemical data from ancient sedimentary successions provide evidence for the progressive evolution of Earth’s atmosphere and oceans1,2,3,4,5,6,7. Key stages in increasing oxygenation are postulated for the Palaeoproterozoic era (∼2.3 billion years ago, Gyr ago) and the late Proterozoic eon (about 0.8 Gyr ago), with the latter implicated in the subsequent metazoan evolutionary expansion8. In support of this rise in oxygen concentrations, a large database1,2,3,9 shows a marked change in the bacterially mediated fractionation of seawater sulphate to sulphide of Δ34S < 25‰ before 1 Gyr to ≥50‰ after 0.64 Gyr. This change in Δ34S has been interpreted to represent the evolution from single-step bacterial sulphate reduction to a combination of bacterial sulphate reduction and sulphide oxidation, largely bacterially mediated3,7,9. This evolution is seen as marking the rise in atmospheric oxygen concentrations and the evolution of non-photosynthetic sulphide-oxidizing bacteria3,7,10. Here we report Δ34S values exceeding 50‰ from a terrestrial Mesoproterozoic (1.18 Gyr old) succession in Scotland, a time period that is at present poorly characterized. This level of fractionation implies disproportionation in the sulphur cycle, probably involving sulphide-oxidizing bacteria, that is not evident from Δ34S data in the marine record1,2,3,9. Disproportionation in both red beds and lacustrine black shales at our study site suggests that the Mesoproterozoic terrestrial environment was sufficiently oxygenated to support a biota that was adapted to an oxygen-rich atmosphere, but had also penetrated into subsurface sediment.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Compilation of published and new sulphur isotope compositions for sedimentary pyrite.
Figure 2: Map of NW Scotland showing outcrop of Stoer Group and sample localities.
Figure 3: Summary stratigraphic section of Stoer and Torridon groups.
Figure 4: Photomicrographs of Stoer Group sulphide/sulphate occurrences in shale host.

Similar content being viewed by others

References

  1. Canfield, D. E. & Teske, A. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382, 127–132 (1996)

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  3. Canfield, D. E. The evolution of the Earth surface sulfur reservoir. Am. J. Sci. 304, 839–861 (2004)

    Article  CAS  ADS  Google Scholar 

  4. Bekker, A. et al. Dating the rise of atmospheric oxygen. Nature 427, 117–120 (2004)

    Article  CAS  ADS  Google Scholar 

  5. Fike, D. A., Grotzinger, J. P., Pratt, L. M. & Summons, R. E. Oxidation of the Ediacaran Ocean. Nature 444, 744–747 (2006)

    Article  CAS  ADS  Google Scholar 

  6. Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008)

    Article  CAS  ADS  Google Scholar 

  7. Lyons, T. W. & Gill, B. C. Ancient sulfur cycling and oxygenation of the early biosphere. Elements 6, 93–99 (2010)

    Article  CAS  Google Scholar 

  8. Runnegar, B. Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 97, 97–111 (1991)

    Article  Google Scholar 

  9. Canfield, D. E. & Raiswell, R. The evolution of the sulfur cycle. Am. J. Sci. 299, 697–723 (1999)

    Article  CAS  ADS  Google Scholar 

  10. Johnston, D. T., Farquhar, J. & Canfield, D. E. Sulfur isotope insights into microbial sulphate reduction: when microbes meet models. Geochim. Cosmochim. Acta 71, 3929–3947 (2007)

    Article  CAS  ADS  Google Scholar 

  11. Wortmann, U., Bernasconi, S. M. & Böttcher, M. E. Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single-step microbial sulfate reduction. Geology 29, 647–650 (2001)

    Article  CAS  ADS  Google Scholar 

  12. Lyons, T. C., Kah, L. C. & Gellatly, A. M. in The Precambrian Earth: Tempos and Events (eds Eriksson, P. G., Altermann, W., Nelson, D. R., Mueller, W. U. & Catuneanu, O.) 421–440 (Elsevier, 2004)

    Google Scholar 

  13. Hurtgen, M. T., Arthur, M. A. & Halverson, G. P. Neoproterozoic sulfur isotopes, the evolution of microbial sulfur species, and the burial efficiency of sulphide as sedimentary pyrite. Geology 33, 41–44 (2005)

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  15. Kah, L. C., Lyons, T. W. & Chesley, J. T. Geochemistry of a 1.2 Ga carbonate-evaporite succession, northern Baffin and Bylot Islands: implications for Mesoproterozoic marine evolution. Precambr. Res. 111, 203–234 (2001)

    Article  CAS  ADS  Google Scholar 

  16. Stewart, A. D. The later Proterozoic Torridonian rocks of Scotland: their sedimentology, geochemistry and origin. Geol. Soc. Mem. No. 24, (2002)

  17. Prave, A. R. Life on land in the Proterozoic: evidence from the Torridonian rocks of northwest Scotland. Geology 30, 811–814 (2002)

    Article  ADS  Google Scholar 

  18. Fry, B., Giblin, A., Dornblaser, M. & Peterson, B. in Geochemical Transformations of Sedimentary Sulfur (eds Vairavamurthy, A. & Schoonens, M. A. A.) 397–410 (American Chemical Society, 1995)

    Book  Google Scholar 

  19. Turnbull, M. J. M., Whitehouse, M. J. & Moorbath, S. New isotopic age determinations for the Torridonian, NW Scotland. J. Geol. Soc. Lond. 153, 955–964 (1996)

    Article  CAS  Google Scholar 

  20. Darabi, M. H. & Piper, J. D. A. Palaeomagnetism of the (Late Mesoproterozoic) Stoer Group, Northwest Scotland: implications for diagenesis, age and relationship to the Grenville Orogeny. Geol. Mag. 141, 15–39 (2004)

    Article  ADS  Google Scholar 

  21. Amor, K., Hesselbo, S. P., Porcelli, D., Thackrey, S. & Parnell, J. A Precambrian proximal ejecta blanket from Scotland. Geology 36, 303–306 (2008)

    Article  CAS  ADS  Google Scholar 

  22. Strauss, H. The sulfur isotopic record of Precambrian sulfates: new data and a critical evaluation of the existing record. Precambr. Res. 63, 225–246 (1993)

    Article  CAS  ADS  Google Scholar 

  23. Sillitoe, R. H., Folk, R. L. & Saric, N. Bacteria as mediators of copper sulfide enrichment during weathering. Science 272, 1153–1155 (1996)

    Article  CAS  ADS  Google Scholar 

  24. Lowry, D., Boyce, A. J., Fallick, A. E., Stephens, W. E. & Grassineau, N. V. Terrane and basement discrimination in northern Britain using sulphur isotopes and mineralogy of ore deposits. Geol. Soc. Lond. Spec. Publ. 248, 133–151 (2005)

    Article  CAS  ADS  Google Scholar 

  25. Machel, H. G. Bacterial and thermochemical sulphate reduction in diagenetic settings — old and new insights. Sedim. Geol. 140, 143–175 (2001)

    Article  CAS  ADS  Google Scholar 

  26. Johnston, D. T., Wolfe-Simon, F., Pearson, A. & Knoll, A. H. Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age. Proc. Natl Acad. Sci. USA 106, 16925–16929 (2009)

    Article  CAS  ADS  Google Scholar 

  27. Poulton, S. W., Fralick, P. W. & Canfield, D. E. Spatial variability in oceanic redox structure 1.8 billion years ago. Nature Geosci. 3, 486–490 (2010)

    Article  CAS  ADS  Google Scholar 

  28. Robinson, B. W. & Kusakabe, M. Quantitative preparation of sulfur dioxide for 34S/32S analyses from sulphides by combustion with cuprous oxide. Anal. Chem. 47, 1179–1181 (1975)

    Article  CAS  Google Scholar 

  29. Coleman, M. L. & Moore, M. P. Direct reduction of sulphates to sulphur dioxide for isotopic analysis. Anal. Chem. 28, 199–260 (1978)

    Google Scholar 

  30. Wagner, T., Boyce, A. J. & Fallick, A. E. Laser combustion analysis of δ34S of sulfosalt minerals: determination of the fractionation systematics and some crystal-chemical considerations. Geochim. Cosmochim. Acta 66, 2855–2863 (2002)

    Article  CAS  ADS  Google Scholar 

Download references

Acknowledgements

We thank D. Fike for criticism of the manuscript; J. Still, J. B. Fulton and C. W. Taylor for technical help. S.S. is funded by the University of Aberdeen. NERC provides funding for the Argon Isotope and Isotope Community Support Facilities, and SUERC is financially supported by the Scottish Universities Consortium.

Author information

Authors and Affiliations

  1. School of Geosciences, University of Aberdeen, Aberdeen AB24 3UE, UK ,

    John Parnell, Stephen Bowden & Sam Spinks

  2. Scottish Universities Environmental Research Centre, East Kilbride, Glasgow G75 0QF, UK ,

    Adrian J. Boyce & Darren Mark

Authors
  1. John Parnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adrian J. Boyce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Darren Mark
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen Bowden
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sam Spinks
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.P. directed the research; A.J.B. performed sulphur isotope analysis; D.M. performed Ar/Ar dating; J.P, S.B. and S.S. undertook field sampling; S.S. and S.B. performed petrographic analysis; J.P, A.B. and D.M. wrote the paper. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to John Parnell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Stoer Group summary and references, Stac Fada Member summary, Ar/Ar methods, Ar/Ar brief discussion and references, Raw Ar/Ar data and step-heating spectrum with inverse and normal isochron plots, Raw sulphur isotope data, diagenetic sulphides and Raw sulphur isotope data, cross-cutting sulphides. (PDF 1003 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parnell, J., Boyce, A., Mark, D. et al. Early oxygenation of the terrestrial environment during the Mesoproterozoic. Nature 468, 290–293 (2010). https://doi.org/10.1038/nature09538

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09538

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology