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.

  • Article
  • Published:

Iron-dependent nitrogen cycling in a ferruginous lake and the nutrient status of Proterozoic oceans

Nature Geoscience volume 10, pages 217–221 (2017)Cite this article

Subjects

Abstract

Nitrogen limitation during the Proterozoic has been inferred from the great expanse of ocean anoxia under low-O2 atmospheres, which could have promoted NO3− reduction to N2 and fixed N loss from the ocean. The deep oceans were Fe rich (ferruginous) during much of this time, yet the dynamics of N cycling under such conditions remain entirely conceptual, as analogue environments are rare today. Here we use incubation experiments to show that a modern ferruginous basin, Kabuno Bay in East Africa, supports high rates of NO3− reduction. Although 60% of this NO3− is reduced to N2 through canonical denitrification, a large fraction (40%) is reduced to NH4+, leading to N retention rather than loss. We also find that NO3− reduction is Fe dependent, demonstrating that such reactions occur in natural ferruginous water columns. Numerical modelling of ferruginous upwelling systems, informed by our results from Kabuno Bay, demonstrates that NO3− reduction to NH4+ could have enhanced biological production, fuelling sulfate reduction and the development of mid-water euxinia overlying ferruginous deep oceans. This NO3− reduction to NH4+ could also have partly offset a negative feedback on biological production that accompanies oxygenation of the surface ocean. Our results indicate that N loss in ferruginous upwelling systems may not have kept pace with global N fixation at marine phosphorous concentrations (0.04–0.13 μM) indicated by the rock record. We therefore suggest that global marine biological production under ferruginous ocean conditions in the Proterozoic eon may thus have been P not N limited.

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: Vertical distribution of selected physical and chemical properties of Kabuno Bay for February 2012.
Figure 2: Rates and pathways in Kabuno Bay for February 2012.
Figure 3: Model outputs describing coupled C, N, S and Fe cycling in an idealized Proterozoic upwelling system.

Similar content being viewed by others

References

  1. Vitousek, P. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).

    Article  Google Scholar 

  2. Codispoti, L. A. et al. The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene? Sci. Mar. 65, 85–105 (2001).

    Article  Google Scholar 

  3. Paulmier, A. & Ruiz-Pino, D. Oxygen minimum zones (OMZs) in the modern ocean. Prog. Oceanogr. 80, 113–128 (2009).

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Fennel, K., Follows, M. & Falkowski, P. G. The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Am. J. Sci. 305, 526–545 (2005).

    Article  Google Scholar 

  6. Godfrey, L. V., Poulton, S. W., Bebout, G. E. & Fralick, P. W. Stability of the nitrogen cycle during development of sulfidic water in the redox-stratified late Paleoproterozoic Ocean. Geology 41, 655–658 (2013).

    Article  Google Scholar 

  7. Canfield, D. E. et al. A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330, 1375–1378 (2010).

    Article  Google Scholar 

  8. Kalvelage, T. et al. Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nat. Geosci. 6, 228–234 (2013).

    Article  Google Scholar 

  9. Johnston, D. T. et al. An emerging picture of Neoproterozoic ocean chemistry: insights from the Chuar Group, Grand Canyon, USA. Earth Planet. Sci. Lett. 290, 64–73 (2010).

    Article  Google Scholar 

  10. Li, C. et al. A stratified redox model for the Ediacaran ocean. Science 328, 80–83 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Reinhard, C. T., Raiswell, R., Scott, C., Anbar, A. D. & Lyons, T. W. A late archean sulfidic sea stimulated by early oxidative weathering of the continents. Science 326, 713–716 (2009).

    Article  Google Scholar 

  13. Poulton, S. W. & Canfield, D. E. Ferruginous conditions: a dominant feature of the ocean through earth’s history. Elements 7, 107–112 (2011).

    Article  Google Scholar 

  14. Straub, K. L., Benz, M., Schink, B. & Widdel, F. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62, 1458–1460 (1996).

    Google Scholar 

  15. Weber, K. A., Urrutia, M. M., Churchill, P. F., Kukkadapu, R. K. & Roden, E. E. Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 8, 100–113 (2006).

    Article  Google Scholar 

  16. Lliros, M. et al. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci. Rep. 5, 13803 (2015).

    Article  Google Scholar 

  17. Lam, P. et al. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl Acad. Sci. USA 106, 4752–4757 (2009).

    Article  Google Scholar 

  18. Jensen, M. M., Petersen, J., Dalsgaard, T. & Thamdrup, B. Pathways, rates, and regulation of N2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. Mar. Chem. 113, 102–113 (2009).

    Article  Google Scholar 

  19. Jensen, M. M. et al. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J. 5, 1660–1670 (2011).

    Article  Google Scholar 

  20. De Brabandere, L. et al. Vertical partitioning of nitrogen-loss processes across the oxic-anoxic interface of an oceanic oxygen minimum zone. Environ. Microbiol. 16, 3041–3054 (2014).

    Article  Google Scholar 

  21. Robertson, E. K., Roberts, K. L., Burdorf, L. D. W., Cook, P. & Thamdrup, B. Dissimilatory nitrate reduction to ammonium coupled to Fe(II) oxidation in sediments of a periodically hypoxic estuary. Limnol. Oceanogr. 61, 365–381 (2016).

    Article  Google Scholar 

  22. Canfield, D. E., Rosing, M. T. & Bjerrum, C. Early anaerobic metabolisms. Phil. Trans. R Soc. B 361, 1819–1834 (2006).

    Article  Google Scholar 

  23. Canfield, D. E. Models of oxic respiration, denitrification and sulfate reduction in zones of coastal upwelling. Geochim. Cosmochim. Acta 70, 5753–5765 (2006).

    Article  Google Scholar 

  24. Boyle, R. A. et al. Nitrogen cycle feedbacks as a control on euxinia in the mid-Proterozoic ocean. Nat. Commun. 4 (2013).

  25. Tyrrell, T. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999).

    Article  Google Scholar 

  26. Jones, C., Nomosatryo, S., Crowe, S. A., Bjerrum, C. J. & Canfield, D. E. Iron oxides, divalent cations, silica, and the early earth phosphorus crisis. Geology 43, 135–138 (2015).

    Article  Google Scholar 

  27. Holland, H. D. The Chemical Evolution of the Atmosphere and Oceans (Princeton Univ. Press, 1984).

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. Vertex–carbon cycling in the northeast Pacific. Deep-Sea Res. 34, 267–285 (1987).

    Article  Google Scholar 

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

    Article  Google Scholar 

  33. Grasshoff, K., Ehrhardt, M., Kremling, K. & Anderson, L. G. Methods of Seawater Analysis 3rd edn (Wiley, 1999).

    Book  Google Scholar 

  34. Fontijn, A., Sabadell, A. J. & Ronco, R. J. Homogeneous chemiluminescent measurement of nitric oxide with ozone—implications for continuous selective monitoring of gaseous air pollutants. Anal. Chem. 42, 575–579 (1970).

    Article  Google Scholar 

  35. Viollier, E., Inglett, P. W., Hunter, K., Roychoudhury, A. N. & Van Cappellen, P. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl. Geochem. 15, 785–790 (2000).

    Article  Google Scholar 

  36. Thamdrup, B. et al. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnol. Oceanogr. 51, 2145–2156 (2006).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank G. Alunga, P. Masilya, P. M. Ishumbisho, B. Kaningini, C. Balagizi, K. Karume, M. Yalire, Djoba, Silas, L. Nyinawamwiza, B. Leporcq, A. Anzil, M.-V. Commarieu, C. Wiking-Antiviakis and L. De Brabandere for help with laboratory and field work. This work was partially supported by Agouron Institute and NSERC discovery grants to S.A.C., and Belgian (FNRS2.4.515.11 and BELSPO SD/AR/02A contracts), Danish (grant no. DNRF53 to D.E.C.) and European (grant no. ERC-StG 240002, for stable isotope measurements) funds. A.V.B. is a senior research associate at the FRS-FNRS. C. Reinhard provided insightful comments.

Author information

Authors and Affiliations

  1. & Atmospheric Sciences Departments, Microbiology & Immunology, and Earth, Ocean, University of British Columbia, Vancouver, BC V6T 1Z3, Canada

    Céline C. Michiels & Sean A. Crowe

  2. Chemical Oceanography Unit, Université de Liège, 4000 Liège, Belgium

    François Darchambeau, Fleur A. E. Roland & Alberto V. Borges

  3. Department of Earth & Environmental Sciences, KU Leuven, 3001 Leuven, Belgium

    Cédric Morana

  4. Microbiology & Immunology Department, Universitat Autònoma de Barcelona, 08193 Barcelona, Spain

    Marc Llirós

  5. Institute of Life Sciences (ISV), Université Catholique de Louvain, 1348 Louvain-la-Neuve, Belgium

    Marc Llirós

  6. Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, 1050 Bruxelles, Belgium

    Tamara García-Armisen & Pierre Servais

  7. Institute of Biology, Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense, Denmark

    Bo Thamdrup & Donald E. Canfield

  8. Université de Recherche en Biologie Environnementale et Évolutive (URBE), Université de Namur, 5000 Namur, Belgium

    Jean-Pierre Descy

Authors
  1. Céline C. Michiels
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. François Darchambeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fleur A. E. Roland
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cédric Morana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marc Llirós
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tamara García-Armisen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bo Thamdrup
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alberto V. Borges
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Donald E. Canfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pierre Servais
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jean-Pierre Descy
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sean A. Crowe
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.D., A.V.B., C.C.M. and S.A.C. designed the experiments. F.D., F.A.E.R., S.A.C. and C.C.M. carried out the experiments. C.C.M. and S.A.C. analysed data and developed the model. C.C.M. and S.A.C. co-wrote the paper. All of the authors contributed to the revision of the paper.

Corresponding author

Correspondence to Sean A. Crowe.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Michiels, C., Darchambeau, F., Roland, F. et al. Iron-dependent nitrogen cycling in a ferruginous lake and the nutrient status of Proterozoic oceans. Nature Geosci 10, 217–221 (2017). https://doi.org/10.1038/ngeo2886

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo2886

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