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:

Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event

Nature Geoscience volume 7, pages 283–286 (2014)Cite this article

Subjects

Abstract

The early Earth was characterized by the absence of oxygen in the ocean–atmosphere system, in contrast to the well-oxygenated conditions that prevail today. Atmospheric concentrations first rose to appreciable levels during the Great Oxidation Event, roughly 2.5–2.3 Gyr ago. The evolution of oxygenic photosynthesis is generally accepted to have been the ultimate cause of this rise, but it has proved difficult to constrain the timing of this evolutionary innovation1,2. The oxidation of manganese in the water column requires substantial free oxygen concentrations, and thus any indication that Mn oxides were present in ancient environments would imply that oxygenic photosynthesis was ongoing. Mn oxides are not commonly preserved in ancient rocks, but there is a large fractionation of molybdenum isotopes associated with the sorption of Mo onto the Mn oxides that would be retained. Here we report Mo isotopes from rocks of the Sinqeni Formation, Pongola Supergroup, South Africa. These rocks formed no less than 2.95 Gyr ago3 in a nearshore setting. The Mo isotopic signature is consistent with interaction with Mn oxides. We therefore infer that oxygen produced through oxygenic photosynthesis began to accumulate in shallow marine settings at least half a billion years before the accumulation of significant levels of atmospheric oxygen.

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: Evidence for Mn oxidation in Precambrian iron formations.
Figure 2: Backscattered electron images and energy-dispersive X-ray spectroscopy major element maps of a representative Mn-rich ([Mn] = 5.8%) sample from the Sinqeni iron formation (TSB07-26-165.42).
Figure 3: Overview of the presented model for Mn–Fe–Mo cycling during deposition of the 2.95-Gyr-old Sinqeni iron formation.

Similar content being viewed by others

References

  1. Farquhar, J., Zerkle, A. L. & Bekker, A. Geological constraints on the origin of oxygenic photosynthesis. Photosynth. Res. 107, 11–36 (2011).

    Article  Google Scholar 

  2. Holland, H. D. The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. B 361, 903–915 (2006).

    Article  Google Scholar 

  3. Mukasa, S. B., Wilson, A. H. & Young, K. R. Geochronological constraints on the magmatic and tectonic development of the Pongola Supergroup (Central Region), South Africa. Precambr. Res. 224, 268–286 (2013).

    Article  Google Scholar 

  4. Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1103 (2008).

    Article  Google Scholar 

  5. Buick, R. When did oxygenic photosynthesis evolve?. Phil. Trans. R. Soc. B 363, 2731–2743 (2008).

    Article  Google Scholar 

  6. Rosing, M. T. & Frei, R. U-rich Archaean sea-floor sediments from Greenland: Indications of 3,700 Ma oxygenic photosynthesis. Earth Planet. Sci. Lett. 217, 237–244 (2004).

    Article  Google Scholar 

  7. Kirschvink, J. L. & Kopp, R. E. Paleoproterozic icehouses and the evolution of oxygen mediating enzymes: The case for a late origin of photosystem-II . Phil. Trans. R. Soc. B 363, 2755–2765 (2008).

    Article  Google Scholar 

  8. Kopp, R. E., Kirschvink, J. L., Hilburn, I. A. & Nash, C. Z. The paleoproterozoic snowball Earth: A climate disaster triggered by the evolution of oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 102, 11131–11136 (2005).

    Article  Google Scholar 

  9. Rashby, S. E., Sessions, A. L., Summons, R. E. & Newman, D. K. Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph. Proc. Natl Acad. Sci. USA 104, 99–104 (2007).

    Article  Google Scholar 

  10. Diem, D. & Stumm, W. Is dissolved Mn(II) being oxidized by O2 in absence of Mn-bacteria or surface catalysts. Geochim. Cosmochim. Acta 48, 1571–1573 (1984).

    Article  Google Scholar 

  11. Tebo, B. M., Johnson, H. A., McCarthy, J. K. & Templeton, A. S. Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 13, 421–428 (2005).

    Article  Google Scholar 

  12. Hansel, C. M., Zeiner, C. A., Santelli, C. M. & Webb, S. M. Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proc. Natl Acad. Sci. USA 109, 12621–12625 (2012).

    Article  Google Scholar 

  13. Learman, D., Voelker, B., Vazquez-Rodriguez, A. & Hansel, C. Formation of manganese oxides by bacterially generated superoxide. Nature Geosci. 4, 95–98 (2011).

    Article  Google Scholar 

  14. Clement, B. G., Luther, G. W. & Tebo, B. M. Rapid, oxygen-dependent microbial Mn(II) oxidation kinetics at sub-micromolar oxygen concentrations in the Black Sea suboxic zone. Geochim. Cosmochim. Acta 73, 1878–1889 (2009).

    Article  Google Scholar 

  15. Anbar, A. D. & Holland, H. D. The photochemistry of manganese and the origin of banded iron formations. Geochim. Cosmochim. Acta 56, 2595–2603 (1992).

    Article  Google Scholar 

  16. Barling, J. & Anbar, A. D. Molybdenum isotope fractionation during adsorption by manganese oxides. Earth Planet. Sci. Lett. 217, 315–329 (2004).

    Article  Google Scholar 

  17. Wasylenki, L. E., Rolfe, B. A., Weeks, C. L., Spiro, T. G. & Anbar, A. D. Experimental investigation of the effects of temperature and ionic strength on Mo isotope fractionation during adsorption to manganese oxides. Geochim. Cosmochim. Acta 72, 5997–6005 (2008).

    Article  Google Scholar 

  18. Goldberg, T., Archer, C., Vance, D. & Poulton, S. W. Mo isotope fractionation during adsorption to Fe (oxyhydr)oxides. Geochim. Cosmochim. Acta 73, 6502–6516 (2009).

    Article  Google Scholar 

  19. Sverjensky, D. A. & Lee, N. The great oxidation event and mineral diversification. Elements 6, 31–36 (2010).

    Article  Google Scholar 

  20. Fralick, P., Davis, D. W. & Kissin, S. A. The age of the Gunflint Formation, Ontario, Canada: Single zircon U–Pb age determinations from reworked volcanic ash. Can. J. Earth Sci. 39, 1085–1091 (2002).

    Article  Google Scholar 

  21. Czaja, A. D. et al. Evidence for free oxygen in the Neoarchean ocean based on coupled iron-molybdenum isotope fractionation. Geochim. Cosmochim. Acta 86, 118–137 (2012).

    Article  Google Scholar 

  22. Machado, A. B. On the origin and age of the Steep Rock buckshot, Ontario, Canada. Chem. Geol. 60, 337–349 (1987).

    Article  Google Scholar 

  23. Hammerbeck, E. C. I. The Usushwana Complex in the Southeastern Transvaal with Special References to its Economic Potential Ph.D. thesis, Univ. Pretoria (1977)

  24. Elworthy, T., Eglington, B. M., Armstrong, R. A. & Moyes, A. B. Rb–Sr isotope constraints on the timing of late to post-Archaean tectonometamorphism affecting the southeastern Kaapvaal Craton. J. Afr. Earth Sci. 30, 641–650 (2000).

    Article  Google Scholar 

  25. Horváth, P., Reinhardt, J., Hofmann, A. & Nagy, G. High-grade metamorphism of ironstones in the Mesoarchaean of southwest Swaziland. Mineral. Petrol. (2014)10.1007/s00710-013-0307-1

  26. Beukes, N. J. & Cairncross, B. A Lithostratigraphic–sedimentological reference profile for the Late Archaean Mozaan Group, Pongola Sequence: Application to sequence stratigraphy and correlation with the Witwatersrand Supergroup. S. Afr. J. Geol. 94, 44–69 (1991).

    Google Scholar 

  27. Planavsky, N. et al. Iron isotope composition of some Archean and Proterozoic iron formations. Geochim. Cosmochim. Acta 80, 158–169 (2012).

    Article  Google Scholar 

  28. Johnson, C. M., Beard, B. L., Klein, C., Beukes, N. J. & Roden, E. E. Iron isotopes constrain biologic and abiologic processes in banded iron formation genesis. Geochim. Cosmochim. Acta 72, 151–169 (2008).

    Article  Google Scholar 

  29. Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999).

    Article  Google Scholar 

  30. Johnson, J. et al. Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc. Natl Acad. Sci. USA 110, 11238–11243 (2013).

    Article  Google Scholar 

  31. David, L. A. & Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011).

    Article  Google Scholar 

  32. Crowe, S. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).

    Article  Google Scholar 

Download references

Acknowledgements

N.J.P. acknowledges financial support from NSF EAR-PF; O.J.R. and D.A. from Europole Mer and ANR-10-LABX-19-01; A.H. and F.O.O. from the NRF of South Africa and Acclaim Exploration; S.V.L. from NSERC-PF and LabexMer-PF; K.O.K. from NSERC; N.J.P., T.W.L., C.T.R. and T.M.J. from NASA Exobiology; and T.W.L. from NSF EAR. C. Delvigne, J. Hancox and N. Hicks provided access to drill core and samples; E. Ponzevera and Y. Germain provided technical assistance.

Author information

Authors and Affiliations

  1. Yale University, New Haven, Connecticut 06520, USA

    Noah J. Planavsky & Xiangli Wang

  2. IFREMER, Plouzané 56470, France

    Dan Asael & Olivier J. Rouxel

  3. University of Johannesburg, Johannesburg 2092, South Africa

    Axel Hofmann, Frantz Ossa Ossa, Albertus J. B. Smith & Nicolas J. Beukes

  4. California Institute of Technology, Pasadena, California 91125, USA

    Christopher T. Reinhard

  5. Institut Universitaire Européen de la Mer, Plouzané 29280, France

    Stefan V. Lalonde

  6. Lawrence University, Appleton, Wisconsin 54911, USA

    Andrew Knudsen

  7. University of Illinois, Urbana-Champaign, Illinois 61820, USA

    Xiangli Wang & Thomas M. Johnson

  8. University of Alberta, Edmonton, Alberta T6G 2R3, Canada

    Ernesto Pecoits & Kurt O. Konhauser

  9. University of California, Riverside, California 92521, USA

    Andrey Bekker & Timothy W. Lyons

Authors
  1. Noah J. Planavsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dan Asael
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Axel Hofmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher T. Reinhard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefan V. Lalonde
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrew Knudsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiangli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Frantz Ossa Ossa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ernesto Pecoits
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Albertus J. B. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Nicolas J. Beukes
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrey Bekker
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Thomas M. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Kurt O. Konhauser
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Timothy W. Lyons
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Olivier J. Rouxel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.J.P. wrote the paper with input from all authors. N.J.P., D.A., O.J.R., A.K., S.V.L., F.O.O., E.P., X.W. and C.T.R. generated data. A.H. and N.J.P. provided samples. N.J.P. and C.T.R. designed the study with input from all authors.

Corresponding author

Correspondence to Noah J. Planavsky.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 5151 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Planavsky, N., Asael, D., Hofmann, A. et al. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nature Geosci 7, 283–286 (2014). https://doi.org/10.1038/ngeo2122

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo2122

This article is cited by

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