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Mineral-catalysed formation of marine NO and N2O on the anoxic early Earth

Nature Geoscience volume 15, pages 1056–1063 (2022)Cite this article

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Abstract

Microbial denitrification converts fixed nitrogen species into gases in extant oceans. However, it is unclear how such transformations occurred within the early nitrogen cycle of the Archaean. Here we demonstrate under simulated Archaean conditions mineral-catalysed reduction of nitrite via green rust and magnetite to reach enzymatic conversion rates. We find that in an Fe2+-rich marine environment, Fe minerals could have mediated the formation of nitric oxide (NO) and nitrous oxide (N2O). Nitrate did not exhibit reactivity in the presence of either mineral or aqueous Fe2+; however, both minerals induced rapid nitrite reduction to NO and N2O. While N2O escaped into the gas phase (63% of nitrite nitrogen, with green rust as the catalyst), NO remained associated with precipitates (7%), serving as a potential shuttle to the benthic ocean. Diffusion and photochemical modelling suggest that marine N2O emissions would have sustained 0.8–6.0 parts per billion of atmospheric N2O without a protective ozone layer. Our findings imply a globally distributed abiotic denitrification process that feasibly aided early microbial life to accrue new capabilities, such as respiratory metabolisms.

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Fig. 1: Molecular NOx– consumption and associated NO and N2O production with Fe minerals or aqueous Fe2+.
Fig. 2: Solid-phase ratios of reduced and oxidized Fe in green rust and magnetite.
Fig. 3: Atmospheric N2O under the influence of mineral-catalysed N2O production in the Archaean ocean.
Fig. 4: Affinity landscapes.
Fig. 5: Schematic of mineral-catalysed NO and N2O formation at the junction of the early nitrogen and iron cycle.

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Data availability

All of the data relating to this manuscript are provided within the manuscript and its Supplementary Information and are available as raw data on the Figshare platform (https://doi.org/10.6084/m9.figshare.20740204.v3) or upon request from the corresponding author.

Code availability

The code for the photochemical model will be shared by the corresponding author upon request.

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Acknowledgements

We thank M. Kirven-Brooks and C. P. McKay for support during the initial experimental phase at the NASA Ames Research Center. We are grateful to K. Weiss, S. Phrasavath, E. Soignard and A. Smith for help with the mineral analytics. We also thank J. G. Lopez for discussions on the diffusion modelling and A. D. Anbar, C. M. Ostrander, J. B. Glass, A. Kappler, M. J. Russell and S. Yoon for feedback on the manuscript. H.C.-Q. and S.B. were supported by the National Aeronautics and Space Administration’s (NASA’s) Nexus for Exoplanet System Science (NExSS) research coordination network at Arizona State University led by S. J. Desch (NNX-15AD53G) and sponsored by NASA’s Science Mission Directorate. S.B. and H.I. received critical funding through the NASA Astrobiology Institute (NAI) Early Career Collaboration Award. H.I. also received funding for this work from the NASA Exoplanets Research Program and NExSS grant NNX-15AQ73G. The research was carried out in part at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with NASA (80NM0018D0004). R.H. was supported in part by NASA’s Exoplanets Research Program grant 80NM0018F0612. S.J.R. acknowledges support from NASA Exobiology (award 80NSSC19K0474) and the National Science Foundation Sedimentary Geology and Paleobiology Program (award 1733598).

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  1. Steffen Buessecker

    Present address: Department of Earth System Science, Stanford University, Stanford, CA, USA

Authors and Affiliations

  1. School of Life Sciences, Arizona State University, Tempe, AZ, USA

    Steffen Buessecker & Hinsby Cadillo-Quiroz

  2. SETI Institute, Mountain View, CA, USA

    Hiroshi Imanaka

  3. NASA Ames Research Center, Mountain View, CA, USA

    Hiroshi Imanaka

  4. School of Earth and Space Exploration, Arizona State University, Tempe, AZ, USA

    Tucker Ely & Stephen J. Romaniello

  5. Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA, USA

    Renyu Hu

  6. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA

    Renyu Hu

  7. Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, TN, USA

    Stephen J. Romaniello

  8. Biodesign Institute, Arizona State University, Tempe, AZ, USA

    Hinsby Cadillo-Quiroz

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Contributions

S.B., H.I. and H.C.-Q. developed overall study objectives and the experimental design. S.B. performed the experiments. S.B., T.E. and S.J.R. conducted the thermodynamics and diffusion modelling. R.H. created the photochemical model. S.B. and H.C.-Q. drafted the manuscript. All authors participated in final revisions of the paper.

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Buessecker, S., Imanaka, H., Ely, T. et al. Mineral-catalysed formation of marine NO and N2O on the anoxic early Earth. Nat. Geosci. 15, 1056–1063 (2022). https://doi.org/10.1038/s41561-022-01089-9

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