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.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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.
References
Mancinelli, R. L. & McKay, C. P. The evolution of nitrogen cycling. Orig. Life Evol. Biosph. 18, 311–325 (1988).
Wong, M. L., Charnay, B. D., Gao, P., Yung, Y. L. & Russell, M. J. Nitrogen oxides in early Earth’s atmosphere as electron acceptors for life’s emergence. Astrobiology 17, 975–983 (2017).
Summers, D. P. & Khare, B. Nitrogen fixation on early Mars and other terrestrial planets: experimental demonstration of abiotic fixation reactions to nitrite and nitrate. Astrobiology 7, 333–341 (2007).
Ranjan, S., Todd, Z. R., Rimmer, P. B., Sasselov, D. D. & Babbin, A. R. Nitrogen oxide concentrations in natural waters on early Earth. Geochem. Geophys. Geosystems 20, 2021–2039 (2019).
Kampschreur, M. J., Kleerebezem, R., de Vet, W. W. J. M. & Loosdrecht, M. C. M. V. Reduced iron induced nitric oxide and nitrous oxide emission. Water Res. 45, 5945–5952 (2011).
Jones, L. C., Peters, B., Pacheco, J. S. L., Casciotti, K. L. & Fendorf, S. Stable isotopes and iron oxide mineral products as markers of chemodenitrification. Environ. Sci. Technol. 49, 3444–3452 (2015).
Grabb, K. C., Buchwald, C., Hansel, C. M. & Wankel, S. D. A dual nitrite isotopic investigation of chemodenitrification by mineral-associated Fe(ii) and its production of nitrous oxide. Geochim. Cosmochim. Acta 196, 388–402 (2017).
Kasting, J. F. in Earth’s Early Atmosphere and Surface Environment 19–28 (Geological Society of America, 2014).
Gough, D. O. in Physics of Solar Variations 21–34 (Springer Dordrecht, 1981).
Stanton, C. L. et al. Nitrous oxide from chemodenitrification: a possible missing link in the Proterozoic greenhouse and the evolution of aerobic respiration. Geobiology 16, 597–609 (2018).
Buick, R. Did the Proterozoic ‘Canfield Ocean’ cause a laughing gas greenhouse? Geobiology 5, 97–100 (2007).
Godfrey, L. V. & Falkowski, P. G. The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci. 2, 725–729 (2009).
Roberson, A. L., Roadt, J., Halevy, I. & Kasting, J. F. Greenhouse warming by nitrous oxide and methane in the Proterozoic Eon. Geobiology 9, 313–320 (2011).
Li, Y., Yamaguchi, A., Yamamoto, M., Takai, K. & Nakamura, R. Molybdenum sulfide: a bioinspired electrocatalyst for dissimilatory ammonia synthesis with geoelectrical current. J. Phys. Chem. C 121, 2154–2164 (2017).
Halevy, I., Alesker, M., Schuster, E. M., Popovitz-Biro, R. & Feldman, Y. A key role for green rust in the Precambrian oceans and the genesis of iron formations. Nat. Geosci. 10, 135–139 (2017).
Sorensen, J. & Thorling, L. Stimulation by lepidocrocite (7-FeOOH) of Fe(ii)-dependent nitrite reduction. Geochim. Cosmochim. Acta 55, 1289–1294 (1991).
Hansen, H., Borggaard, O. K. & Sorensen, J. Evaluation of the free energy of formation of Fe(ii)–Fe(iii) hydroxide-sulphate (green rust) and its reduction of nitrite. Geochim. Cosmochim. Acta 58, 2599–2608 (1994).
Ottley, C. J., Davison, W. & Edmunds, W. M. Chemical catalysis of nitrate reduction by iron (ii). Geochim. Cosmochim. Acta 61, 1819–1828 (1997).
Zegeye, A. et al. Green rust formation controls nutrient availability in a ferruginous water column. Geology 40, 599–602 (2012).
Babbin, A. R., Bianchi, D., Jayakumar, A. & Ward, B. B. Rapid nitrous oxide cycling in the suboxic ocean. Science 348, 1127–1129 (2015).
Ji, Q., Babbin, A. R., Jayakumar, A., Oleynik, S. & Ward, B. B. Nitrous oxide production by nitrification and denitrification in the Eastern Tropical South Pacific oxygen minimum zone. Geophys. Res. Lett. 42, 10755–10764 (2015).
Gordon, A. D. et al. Reduction of nitrite and nitrate on nano-dimensioned FeS. Orig. Life Evol. Biosph. 43, 305–322 (2013).
Llirós, M. et al. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci. Rep. 5, 13803 (2015).
Swanner, E. D. et al. Modulation of oxygen production in Archaean oceans by episodes of Fe(ii) toxicity. Nat. Geosci. 8, 126–130 (2015).
Sumner, D. Y. Carbonate precipitation and oxygen stratification in late Archean seawater as deduced from facies and stratigraphy of the Gamohaan and Frisco formations, Transvaal Supergroup, South Africa. Am. J. Sci. 297, 455–487 (1997).
Sumner, D. Y. & Grotzinger, J. P. Were kinetics of Archean calcium carbonate precipitation related to oxygen concentration? Geology 24, 119–122 (1996).
Battaglia, G. & Joos, F. Marine N2O emissions from nitrification and denitrification constrained by modern observations and projected in multimillennial global warming simulations. Glob. Biogeochem. Cycles 32, 92–121 (2018).
Hu, R., Seager, S. & Bains, W. Photochemistry in terrestrial exoplanet atmospheres. I. Photochemistry model and benchmark cases. Astrophys J. 761, 166 (2012).
Kaiser, J., Röckmann, T., Brenninkmeijer, C. A. M. & Crutzen, P. J. Wavelength dependence of isotope fractionation in N2O photolysis. Atmos. Chem. Phys. 3, 303–313 (2003).
Airapetian, V. S., Glocer, A., Gronoff, G., Hebrard, G. & Danchi, W. Prebiotic chemistry and atmospheric warming of early Earth by an active young Sun. Nat. Geosci. 9, 452–455 (2016).
Wolf, E. T. & Toon, O. B. Fractal organic hazes provided an ultraviolet shield for early Earth. Science 328, 1266–1268 (2010).
Catling, D. C., Zahnle, K. J. & McKay, C. P. Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839–843 (2001).
Laneuville, M., Kameya, M. & Cleaves, H. J. Earth without life: a systems model of a global abiotic nitrogen cycle. Astrobiology 18, 897–914 (2018).
Hu, R. & Diaz, H. D. Stability of nitrogen in planetary atmospheres in contact with liquid water. Astrophys J. 886, 126 (2019).
Saito, M. A. et al. Abundant nitrite-oxidizing metalloenzymes in the mesopelagic zone of the tropical Pacific Ocean. Nat. Geosci. 13, 355–362 (2020).
Summers, D. P. & Chang, S. Prebiotic ammonia from reduction of nitrite by iron (ii) on the early Earth. Nature 365, 630–633 (1993).
Brandes, J. A. et al. Abiotic nitrogen reduction on the early Earth. Nature 395, 365–367 (1998).
Nishizawa, M. et al. Stable abiotic production of ammonia from nitrate in komatiite-hosted hydrothermal systems in the Hadean and Archean oceans. Minerals 11, 321 (2021).
Halevy, I. & Bachan, A. The geologic history of seawater pH. Science 355, 1069–1071 (2017).
Harman, C. E. et al. Abiotic O2 levels on planets around F, G, K, and M stars: effects of lightning-produced catalysts in eliminating oxygen false positives. Astrophys J. 866, 56 (2018).
Mather, T. A., Pyle, D. M. & Allen, A. G. Volcanic source for fixed nitrogen in the early Earth’s atmosphere. Geology 32, 905–908 (2004).
Kasting, J. F. Bolide impacts and the oxidation state of carbon in the Earth’s early atmosphere. Orig. Life Evol. Biosph. 20, 199–231 (1990).
Ducluzeau, A.-L. et al. Was nitric oxide the first deep electron sink? Trends Biochem. Sci. 34, 9–15 (2009).
Viebrock, A. & Zumft, W. G. Molecular cloning, heterologous expression, and primary structure of the structural gene for the copper enzyme nitrous oxide reductase from denitrifying Pseudomonas stutzeri. J. Bacteriol. 170, 4658–4668 (1988).
Chen, J. & Strous, M. Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution. Biochim. Biophys. Acta Bioenerg. 1827, 136–144 (2013).
Suharti, S. & de Vries, S. Membrane-bound denitrification in the Gram-positive bacterium Bacillus azotoformans. Biochem. Soc. Trans. 33, 130–133 (2005).
Saraste, M. & Castresana, J. Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett. 341, 1–4 (1994).
Sousa, F. L. et al. The superfamily of heme–copper oxygen reductases: types and evolutionary considerations. Biochim. Biophys. Acta Bioenerg. 1817, 629–637 (2012).
Yoon, S. et al. Nitrous oxide reduction kinetics distinguish bacteria harboring clade I NosZ from those harboring clade II NosZ. Appl. Environ. Microbiol. 82, 3793–3800 (2016).
Heinrich, T. A. et al. Biological nitric oxide signalling: chemistry and terminology. Br. J. Pharmacol. 169, 1417–1429 (2013).
Santana, M. M., Gonzalez, J. M. & Cruz, C. Nitric oxide accumulation: the evolutionary trigger for phytopathogenesis. Front. Microbiol. 8, 1947 (2017).
Nikeleit, V. et al. Inhibition of photoferrotrophy by nitric oxide in ferruginous environments. Preprint at EarthArXiv https://doi.org/10.31223/X5XS60 (2021).
Drummond, J. T. & Matthews, R. G. Nitrous oxide degradation by cobalamin-dependent methionine synthase: characterization of the reactants and products in the inactivation reaction. Biochemistry 33, 3732–3741 (1994).
Drummond, J. T. & Matthews, R. G. Nitrous oxide inactivation of cobalamin-dependent methionine synthase from Escherichia coli: characterization of the damage to the enzyme and prosthetic group. Biochemistry 33, 3742–3750 (1994).
Matthews, R. G. Cobalamin-dependent methyltransferases. Acc. Chem. Res. 34, 681–689 (2001).
Buessecker, S. et al. Microbial communities and interactions of nitrogen oxides with methanogenesis in diverse peatlands of the Amazon basin. Front. Microbiol. 12, 659079 (2021).
McDonnell, A. M. P. & Buesseler, K. O. Variability in the average sinking velocity of marine particles. Limnol. Oceanogr. 55, 2085–2096 (2010).
Krissansen-Totton, J., Olson, S. & Catling, D. C. Disequilibrium biosignatures over Earth history and implications for detecting exoplanet life. Sci. Adv. 4, eaao5747 (2018).
Nicholls, J. C., Davies, C. A. & Trimmer, M. High‐resolution profiles and nitrogen isotope tracing reveal a dominant source of nitrous oxide and multiple pathways of nitrogen gas formation in the central Arabian Sea. Limnol. Oceanogr. 52, 156–168 (2007).
Dalsgaard, T., Thamdrup, B., Farías, L. & Revsbech, N. P. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol. Oceanogr. 57, 1331–1346 (2012).
Löscher, C. R. et al. Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9, 2419–2429 (2012).
Bourbonnais, A. et al. N2O production and consumption from stable isotopic and concentration data in the Peruvian coastal upwelling system. Glob. Biogeochem. Cycles 31, 678–698 (2017).
Frame, C. H. & Casciotti, K. L. Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosciences 7, 2695–2709 (2010).
Zafiriou, O. C. & McFarland, M. Nitric oxide from nitrite photolysis in the central equatorial Pacific. J. Geophys. Res. Atmos. 86, 3173–3182 (1981).
Liu, C.-Y. et al. Determination of dissolved nitric oxide in coastal waters of the Yellow Sea off Qingdao. Ocean Sci. 13, 623–632 (2017).
Martens-Habbena, W. et al. The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger. Environ. Microbiol. 17, 2261–2274 (2015).
Li, Y.-L., Konhauser, K. O. & Zhai, M. The formation of primary magnetite in the early Archean oceans. Earth Planet. Sci. Lett. 466, 103–114 (2017).
Byrne, J. M. et al. Redox cycling of Fe(ii) and Fe(iii) in magnetite by Fe-metabolizing bacteria. Science 347, 1473–1476 (2015).
Pearce, C. I. et al. Synthesis and properties of titanomagnetite (Fe3–xTixO4) nanoparticles: a tunable solid-state Fe(ii/iii) redox system. J. Colloid Interface Sci. 387, 24–38 (2012).
Williams, A. G. B. & Scherer, M. M. Kinetics of Cr(vi) reduction by carbonate green rust. Environ. Sci. Technol. 35, 3488–3494 (2001).
Sun, Z.-X., Su, F.-W., Forsling, W. & Samskog, P.-O. Surface characteristics of magnetite in aqueous suspension. J. Colloid Interface Sci. 197, 151–159 (1998).
Anbar, A. D. & Holland, H. D. The photochemistry of manganese and the origin of banded iron formations. Geochim. Cosmochim. Acta 56, 2595–2603 (1992).
Miranda, K. M., Espey, M. G. & Wink, D. A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62–71 (2001).
Kandeler, E. & Gerber, H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68–72 (1988).
Stookey, L. L. Ferrozine—a new spectrophotometric reagent for iron. Anal. Chem. 42, 779–781 (1970).
Hu, R., Seager, S. & Bains, W. Photochemistry in terrestrial exoplanet atmospheres. II. H2S and SO2 photochemistry in anoxic atmospheres. Astrophys. J. 769, 6 (2013).
Hu, R. Atmospheric photochemistry, surface features, and potential biosignature gases of terrestrial exoplanets. PhD thesis, Massachusetts Institute of Technology (2013).
Catling, D. C. & Zahnle, K. J. The Archean atmosphere. Sci. Adv. 6, eaax1420 (2020).
Claire, M. W. et al. The evolution of solar flux from 0.1 nm to 160 μm: quantitative estimates for planetary studies. Astrophys. J. 757, 95 (2012).
Ranjan, S. et al. Photochemistry of anoxic abiotic habitable planet atmospheres: impact of new H2O cross sections. Astrophys. J. 896, 148 (2020).
Massie, S. T. & Hunten, D. M. Stratospheric eddy diffusion coefficients from tracer data. J. Geophys. Res. Atmos. 86, 9859–9868 (1981).
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).
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Geoscience thanks Manabu Nishizawa, Sarah Rugheimer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Rebecca Neely, in collaboration with the Nature Geoscience team.
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 text, Figs. 1–8, Tables 1–5 and Supplementary References.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41561-022-01089-9
This article is cited by
-
Abiotic path of Archean nitrogen
Nature Geoscience (2022)