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.

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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.

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  1. Microbiology & Immunology, and Earth, Ocean, & Atmospheric Sciences Departments, 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


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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.

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The authors declare no competing financial interests.

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Correspondence to Sean A. Crowe.

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