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.

Ammonium availability in the Late Archaean nitrogen cycle

Nature Geoscience volume 12, pages 553–557 (2019)Cite this article

Subjects

Abstract

The bioavailability of essential nutrients such as nitrogen and phosphorus has fluctuated with the chemical evolution of Earth surface environments over geological timescales. However, significant uncertainty remains over the evolution of Earth’s early nitrogen cycle, particularly how and when it responded to the evolution of oxygenic photosynthesis. Here we apply multi-proxy geochemical analyses (Fe speciation, δ13C and δ15N) to exceptionally well-preserved shales from the approximately 2.7 billion year old Manjeri Formation in the Belingwe Greenstone Belt, Zimbabwe, to evaluate the redox status of Earth’s early nitrogen cycle and decipher feedbacks associated with the initial stages of planetary oxygenation. These continental shelf sediments were previously linked to early cyanobacterial oxygen production, and provide a direct test of conflicting hypotheses concerning the importance of nitrogen oxyanions in the Late Archaean era. Our data reveal a dominantly anaerobic marine nitrogen cycle in which ammonium-replete ferruginous waters underlay an ephemeral oxygen oasis. Driven by the emergence of oxygenic photosynthesis, increased primary productivity could have periodically strengthened export production, which allowed for the accumulation of ammonium in the water column during organic matter degradation. Restricted oxygen availability could have allowed the upwelling ammonium to reach the photic zone to provide ample nitrogen to fuel a prolific Late Archaean biosphere.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Fig. 1: Lithological and geochemical data from the 2.7 Ga Manjeri Formation.
Fig. 2: Modelled δ15N values that can reproduce temporal trends in the rock record.

Similar content being viewed by others

Data availability

The authors declare that all data supporting the findings of this study are available within the article and its supplementary information files.

References

  1. Galloway, J. N. in Biogeochem istry (eds Karl, D. M. and Schlesinger, W. H.) 475–498 (Elsevier, 2014).

  2. Navarro-Gonzalez, R., McKay, C. P. & Mvondo, D. N. A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412, 61–64 (2001).

    Article  Google Scholar 

  3. Stüeken, E. E., Buick, R., Guy, B. & Koehler, M. C. Isotopic evidence for biological nitrogen fixation by Mo-nitrogenase from 3.2 Gyr. Nature 520, 666–669 (2015).

    Article  Google Scholar 

  4. Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).

    Article  Google Scholar 

  5. Dalsgaard, T., Thamdrup, B., Farias, L. & Revsbech, N. P. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol. Oceanogr. 57, 1331–1346 (2012).

    Article  Google Scholar 

  6. Zerkle, A. L. et al. Onset of the aerobic nitrogen cycle during the Great Oxidation Event. Nature 542, 465–467 (2017).

    Article  Google Scholar 

  7. Luo, G. et al. Rapid oxygenation of Earth’s atmosphere 2.33 billion years ago. Sci. Adv. 2, e1600134 (2016).

    Article  Google Scholar 

  8. Baursachs, T. et al. Nitrogen isotopic fractionation associated with growth on dinitrogen gas and nitrate by cyanobacteria. Limnol. Oceanogr. 54, 1403–1411 (2009).

    Article  Google Scholar 

  9. Zhang, X., Sigman, D. M., Morel, F. M. M. & Kraepiel, A. M. L. Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia. Proc. Natl Acad. Sci. USA 111, 4782–4787 (2014).

    Article  Google Scholar 

  10. Zhang, X. et al. Alternative nitrogenase activity in the environment and nitrogen cycle implications. Biogeochemistry 127, 189–198 (2016).

    Article  Google Scholar 

  11. Boyd, E. S. & Peters, J. W. New insights into the evolutionary history of biological nitrogen fixation. Front. Microbiol. 4, 201 (2013).

    Google Scholar 

  12. Hoch, M. P., Fogel, M. L. & Kirchman, D. L. Isotope fractionation associated with ammonium uptake by a marine bacterium. Limnol. Oceanogr. 37, 1447–1459 (1992).

    Article  Google Scholar 

  13. Sigman, D. M., Karsh, K. L. & Casciotti, K. L. in Encyclopedia of Oce an Sciences (eds Steele, J. H., Thorpe, S. A. & Turekian, K. K.) 40–54 (Academic, 2009).

  14. Brunner, B. et al. Nitrogen isotope effects induced by anammox bacteria. Proc. Natl Acad. Sci. USA 110, 18994–18999 (2013).

    Article  Google Scholar 

  15. De Pol-Holz, R., Robinson, R. S., Hebbeln, D., Sigman, D. M. & Ulloa, O. Controls on sedimentary nitrogen isotopes along the Chile margin. Deep-Sea Res. Part II 56, 1100–1112 (2009).

    Google Scholar 

  16. Kipp, M. A., Stüeken, E. E., Yun, M., Bekker, A. & Buick, R. Pervasive aerobic nitrogen cycling in the surface ocean across the Paleoproterozoic era. Earth Planet. Sci. Lett. 500, 117–126 (2018).

    Article  Google Scholar 

  17. Garvin, J., Buick, R., Anbar, A. D., Arnold, G. L. & Kaufman, A. J. Isotopic evidence for an aerobic nitrogen cycle in the latest Archaean. Science 323, 1045–1048 (2009).

    Article  Google Scholar 

  18. Godfrey, L. V. & Falkowski, P. G. The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci. 2, 275–279 (2009).

    Article  Google Scholar 

  19. Bolhar, R., Hofmann, A., Woodhead, J., Hergt, J. & Dirks, P. Pb- and Nd-isotope systematics of stromatolitic limestones from the 2.7 Ga Ngezi Group of the Belingwe Greenstone Belt: constraints on timing of deposition and provenance. Precambrian Res. 114, 277–294 (2002).

    Article  Google Scholar 

  20. Grassineau, N. V., Abell, P., Appel, P. W. U., Lowry, D. & Nisbet, E. G. Early life signatures in sulfur and carbon isotopes from Isua, Barberton, Wabigoon (Steep Rock) and Belingwe Greenstone Belts (3.8 to 2.7 Ga). Geol. Soc. Am. Mem. 198, 33–52 (2006).

    Google Scholar 

  21. Abell, P. I., McClory, J., Martin, A. & Nisbet, E. G. Archaean stromatolites from the Ngesi Group, Belingwe Greenstone Belt, Zimbabwe; preservation and stable isotopes—preliminary results. Precambrian Res. 27, 357–383 (1985).

    Article  Google Scholar 

  22. Nisbet, E. G. et al. Uniquely fresh 2.7 Ga komatiites from the Belingwe greenstone belt, Zimbabwe. Geology 15, 1147–1150 (1987).

    Article  Google Scholar 

  23. Stüeken, E. E., Zaloumis, J., Meixnerova, J. & Buick, R. Differential metamorphic effects on nitrogen isotopes in kerogen extracts and bulk rocks. Geochim. Cosmochim. Acta 217, 80–94 (2017).

    Article  Google Scholar 

  24. Poulton, S. W. & Canfield, D. E. Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates. Chem. Geol. 214, 209–221 (2005).

    Article  Google Scholar 

  25. Eickmann, B. Isotopic evidence for oxygenated Mesoarchean shallow oceans. Nat. Geosci. 11, 133–138 (2018).

    Article  Google Scholar 

  26. Habicht, K. S. & Canfield, D. E. Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments. Geochim. Cosmochim. Acta 61, 5351–5361 (1997).

    Article  Google Scholar 

  27. Thomazo, C., Grassineau, N. V., Nisbet, E. G., Peters, M. & Strauss, H. Multiple sulfur and carbon isotope composition of sediments from the Belingwe Greenstone Belt (Zimbabwe): a biogenic methane regulation on mass independent fractionation of sulfur during the Neoarchean? Geochim. Cosmochim. Acta 121, 120–138 (2013).

    Article  Google Scholar 

  28. Thomazo, C., Ader, M. & Philippot, P. Extreme 15N-enrichments in 2.72-Gyr-old sediments: evidence for a turning point in the nitrogen cycle. Geobiology 9, 107–120 (2011).

    Article  Google Scholar 

  29. Stüeken, E. E., Buick, R. & Schauer, A. J. Nitrogen isotope evidence for alkaline lakes on late Archaean continents. Earth Planet. Sci. Lett. 411, 1–10 (2015).

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Reinhard, C. T. et al. The evolution of the global phosphorus cycle. Nature 467, 1088–1090 (2016).

    Google Scholar 

  32. Izon, G. et al. Biological regulation of atmospheric chemistry en route to planetary oxygenation. Proc. Natl Acad. Sci. USA 114, 2571–2579 (2017).

    Article  Google Scholar 

  33. Canfield, D. E., Raiswell, R., Westrich, J. T., Reaves, C. M. & Berner, R. A. The use of chromium reduction in the analysis of reduced inorganic sulfur in sediments and shales. Chem. Geol. 54, 149–155 (1986).

    Article  Google Scholar 

  34. Mettam, C. et al. High-frequency fluctuations in redox conditions during the latest Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 485, 210–223 (2017).

    Article  Google Scholar 

  35. Clarkson, M. O., Poulton, S. W., Guilbaud, R. & Wood, R. A. Assessing the utility of Fe/Al and the Fe-speciation to record water column redox conditions in carbonate-rich sediments. Chem. Geol. 382, 111–122 (2014).

    Article  Google Scholar 

  36. Slotznick, S. P., Eiler, J. M. & Fischer, W. W. The effect of metamorphism on iron mineralogy and the iron speciation redox proxy. Geochim. Cosmochim. Acta 224, 96–115 (2018).

    Article  Google Scholar 

  37. Grassineau, N. V. High-precision EA-IRMS analysis of S and C isotopes in geological materials. Appl. Geochem. 21, 756–765 (2006).

    Article  Google Scholar 

  38. Coplen, T. B. et al. New guidelines for delta C-13 measurements. Anal. Chem. 78, 2439–2441 (2006).

    Article  Google Scholar 

  39. Polissar, P. J., Fulton, J. M., Junium, C. K., Turich, C. H. & Freeman, K. H. Measurement of 13C and 15N isotopic composition on nanomolar quantities of C and N. Anal. Chem. 81, 755–763 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported financially by Natural Environment Research Council Standard Grants NE/M001156/1 (A.L.Z., E.G.N. and N.V.G.) and NE/J023485/2 (A.L.Z.), and the National Science Foundation NSF EAR-1455258 (C.K.J.). G.I. acknowledges continued support from the Simons Foundation (SCOL:290361) during the final drafts of the manuscript. The authors thank M. Hunter for help in logging the NERCMAR core, D. Herd for assistance with petrography, A. Calder for assistance with X-ray fluorescence analyses, A. Prave for thought-provoking discussion on the Manjeri Formation strata, and T. Laakso, C. Thomazo and M. Ader for constructive comments on previous versions of the manuscript.

Author information

Author notes

  1. G. Izon

    Present address: Department of Earth, Atmospheric & Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

  2. Unaffiliated: anthony.martin2107@gmail.com.

Authors and Affiliations

  1. School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, Fife, UK

    J. Yang, G. Izon, C. Mettam & A. L. Zerkle

  2. Department of Earth Sciences, Syracuse University, Heroy Geology Laboratory, New York, NY, USA

    C. K. Junium

  3. Department of Earth Sciences, Royal Holloway, University of London, Egham, UK

    N. V. Grassineau & E. G. Nisbet

Authors
  1. J. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. K. Junium
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. V. Grassineau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. G. Nisbet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Izon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Mettam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. L. Zerkle
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.L.Z. and E.G.N. conceived the study; J.Y., N.V.G., E.G.N. and A.M. collected the samples; J.Y., C.K.J., N.V.G., G.I. and C.M. processed the samples and performed geochemical analyses; J.Y., A.L.Z. and C.K.J. interpreted the data and wrote the manuscript with input from all the co-authors.

Corresponding author

Correspondence to A. L. Zerkle.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary sample information; Supplementary Figs. 1–5 and Supplementary Tables 1–3.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, J., Junium, C.K., Grassineau, N.V. et al. Ammonium availability in the Late Archaean nitrogen cycle. Nat. Geosci. 12, 553–557 (2019). https://doi.org/10.1038/s41561-019-0371-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-019-0371-1

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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