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Onset of the aerobic nitrogen cycle during the Great Oxidation Event

Abstract

The rise of oxygen on the early Earth (about 2.4 billion years ago)1 caused a reorganization of marine nutrient cycles2,3, including that of nitrogen, which is important for controlling global primary productivity. However, current geochemical records4 lack the temporal resolution to address the nature and timing of the biogeochemical response to oxygenation directly. Here we couple records of ocean redox chemistry with nitrogen isotope (15N/14N) values from approximately 2.31-billion-year-old shales5 of the Rooihoogte and Timeball Hill formations in South Africa, deposited during the early stages of the first rise in atmospheric oxygen on the Earth (the Great Oxidation Event)6. Our data fill a gap of about 400 million years in the temporal 15N/14N record4 and provide evidence for the emergence of a pervasive aerobic marine nitrogen cycle. The interpretation of our nitrogen isotope data in the context of iron speciation and carbon isotope data suggests biogeochemical cycling across a dynamic redox boundary, with primary productivity fuelled by chemoautotrophic production and a nitrogen cycle dominated by nitrogen loss processes using newly available marine oxidants. This chemostratigraphic trend constrains the onset of widespread nitrate availability associated with ocean oxygenation. The rise of marine nitrate could have allowed for the rapid diversification and proliferation of nitrate-using cyanobacteria and, potentially, eukaryotic phytoplankton.

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Figure 1: Secular trend in sedimentary δ15N over early Earth history.
Figure 2: Lithological and geochemical data for core EBA-2.

References

  1. 1

    Bekker, A. et al. Dating the rise of atmospheric oxygen. Nature 427, 117–120 (2004)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Beaumont, V. & Robert, F. Nitrogen isotope ratios of kerogens in Precambrian cherts: a record of the evolution of atmosphere chemistry? Precambr. Res . 96, 63–82 (1999)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Bekker, A. & Holland, H. D. Oxygen overshoot and recovery during the early Paleoproterozoic. Earth Planet. Sci. Lett . 317–318, 295–304 (2012)

    ADS  Article  Google Scholar 

  4. 4

    Stüeken, E. E., Kipp, M. A., Koehler, M. C. & Buick, R. The evolution of Earth’s biogeochemical nitrogen cycle. Earth Sci. Rev . 160, 220–239 (2016)

    Article  Google Scholar 

  5. 5

    Rasmussen, B., Bekker, A. & Fletcher, I. R. Correlations of Paleoproterozoic glaciations based on U-Pb zircon ages for tuff beds in the Transvaal and Huronian Supergroups. Earth Planet. Sci. Lett . 382, 173–180 (2013)

    ADS  CAS  Article  Google Scholar 

  6. 6

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

    ADS  Article  Google Scholar 

  7. 7

    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)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Wada, E. in Isotope Marine Chemistry (eds Goldberg, E. D., Horibe, Y. & Saruhashi, K. ) 375–398 (Uchida Rokakuho, 1980)

  9. 9

    Zerkle, A. L., Junium, C. K., Canfield, D. E. & House, C. H. Production of 15N-depleted biomass during cyanobacterial N2-fixation at high Fe concentrations. J. Geophys. Res. 113, G03014 (2008)

  10. 10

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

    ADS  CAS  Article  Google Scholar 

  11. 11

    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)

    ADS  CAS  Article  Google Scholar 

  12. 12

    McCready, R. G. L., Gould, W. D. & Barendregt, R. W. Nitrogen isotope fractionation during the reduction of NO3 to NH4+ by Desulfovibrio sp. Can. J. Microbiol . 29, 231–234 (1983)

    CAS  Article  Google Scholar 

  13. 13

    Peters, K. E., Sweeney, R. E. & Kaplan, I. R. Correlation of carbon and nitrogen stable isotope ratios in sedimentary organic matter. Limnol. Oceanogr . 23, 598–604 (1978)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Ader, M. et al. Interpretation of the nitrogen isotopic composition of Precambrian sedimentary rocks: assumptions and perspectives. Chem. Geol . 429, 93–110 (2016)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Farquhar, J., Zerkle, A. L. & Bekker, A. Geological constraints on the origin of oxygenic photosynthesis. Photosynth. Res . 107, 11–36 (2011)

    CAS  Article  Google Scholar 

  16. 16

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

    ADS  CAS  Article  Google Scholar 

  17. 17

    Godfrey, L. V. & Falkowski, P. G. The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci . 2, 735–729 (2009)

    ADS  Article  Google Scholar 

  18. 18

    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)

    CAS  Article  Google Scholar 

  19. 19

    Busigny, V., Lebeau, O., Ader, M., Krapez, B. & Bekker, A. Nitrogen cycle in the Late Archean ferruginous ocean. Chem. Geol . 362, 115–130 (2013)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Pavlov, A. A. & Kasting, J. F. Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27–41 (2002)

    ADS  CAS  Article  Google Scholar 

  21. 21

    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)

    ADS  CAS  Article  Google Scholar 

  22. 22

    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)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Coetzee, L. L., Beukes, N. J., Gutzmer, J. & Kakegawa, T. Links of organic carbon cycling and burial to depositional depth gradients and establishment of a snowball Earth at 2.3Ga. Evidence from the Timeball Hill Formation, Transvaal Supergroup, South Africa. S. Afr. J. Geol . 109, 109–122 (2006)

    CAS  Article  Google Scholar 

  24. 24

    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. II 56, 1042–1054 (2009)

    ADS  CAS  Article  Google Scholar 

  25. 25

    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)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Stüeken, E. E. A test of the nitrogen-limitation hypothesis for retarded eukaryote radiation: nitrogen isotopes across a Mesoproterozoic basinal profile. Geochim. Cosmochim. Acta 120, 121–139 (2013)

    ADS  Article  Google Scholar 

  27. 27

    Papineau, D. et al. High primary productivity and nitrogen cycling after the Paleoproterozoic phosphogenic event in the Aravalli Supergroup, India. Precambr. Res . 171, 37–56 (2009)

    ADS  CAS  Article  Google Scholar 

  28. 28

    Kump, L. R. et al. Isotopic evidence for massive oxidation of organic matter following the Great Oxidation Event. Science 334, 1694–1696 (2011)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Farquhar, J., Zerkle, A. L. & Bekker, A. in Treatise in Geochemistry: Reference Module in Earth Systems and Environmental Sciences (eds Holland, H. D. & Turekian, K. ) Vol. 6, 91–138 (Elsevier, 2014)

    Article  Google Scholar 

  30. 30

    Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014)

    ADS  CAS  Article  Google Scholar 

  31. 31

    Thomazo, C. & Papineau, D. Biogeochemical cycling of nitrogen on the early Earth. Elements 9, 345–351 (2013)

    CAS  Article  Google Scholar 

  32. 32

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

    ADS  Article  Google Scholar 

  33. 33

    McKirdy, D. M. & Powell, T. G. Metamorphic alteration of carbon isotopic composition in ancient sedimentary organic matter: new evidence from Australia. Geology 2, 591–595 (1974)

    ADS  CAS  Article  Google Scholar 

  34. 34

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

    CAS  Article  Google Scholar 

  35. 35

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

    CAS  Article  Google Scholar 

  36. 36

    Boyd, S. R. & Philippot, P. Precambrian ammonium biogeochemistry: a study of the Moine metasediments, Scotland. Chem. Geol . 144, 257–268 (1998)

    ADS  CAS  Article  Google Scholar 

  37. 37

    Robinson, R. S. et al. A review of nitrogen isotopic alteration in marine sediments. Paleoceanography 27, http://dx.doi.org/10.1029/2012PA002321 (2012)

  38. 38

    Bebout, G. E. & Fogel, M. L. Nitrogen-isotope compositions of metasedimentary rocks in the Catalina Schist, California: implications for metamorphic devolatilization history. Geochim. Cosmochim. Acta 56, 2839–2849 (1992)

    ADS  CAS  Article  Google Scholar 

  39. 39

    Ader, M., Boudou, J.-P., Javoy, M., Goffe, B. & Daniels, E. Isotope study of organic nitrogen of Westphalian anthracites from the Western Middle field of Pennsylvania (U.S.A.) and from the Bramsche Massif (Germany). Org. Geochem . 29, 315–323 (1998)

    CAS  Article  Google Scholar 

  40. 40

    Schimmelmann, A. & Lis, G. P. Nitrogen isotopic exchange during maturation of organic matter. Org. Geochem . 41, 63–70 (2010)

    CAS  Article  Google Scholar 

  41. 41

    Hoering, T. C. & Moore, H. E. The isotopic compositions of the nitrogen in natural gases and associated crude oils. Geochim. Cosmochim. Acta 13, 225–232 (1958)

    ADS  CAS  Article  Google Scholar 

  42. 42

    Murty, S. V. S. Noble-gases and nitrogen in natural gases from Gujarat, India. Chem. Geol . 94, 229–240 (1992)

    ADS  CAS  Article  Google Scholar 

  43. 43

    Sumner, D. Y. et al. Beukes, N. J. Sequence stratigraphic development of the Neoarchean Transvaal carbonate platform, Kaapvaal Craton, South Africa. S. Afr. J. Geol. 109, 11–22 (2006)

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported financially by a Natural Environment Research Council Fellowship (number NE/H016805 to A.L.Z.). We thank the Council for Geoscience in South Africa and the staff at the National Core Library in Donkerhoek for facilitating access to the core materials, and M. Yun for assistance with stable isotope analyses at the University of Manitoba.

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Authors

Contributions

A.L.Z. and S.W.P. conceived the study. S.W.P. and A.B. collected the samples. A.L.Z., S.W.P., R.J.N., C.M. and C.K.J. processed samples and performed geochemical analyses. M.W.C. provided statistical analyses of the global database. A.L.Z. interpreted the data and wrote the manuscript with input from all coauthors.

Corresponding author

Correspondence to Aubrey L. Zerkle.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Results from statistical analysis of the δ15N database.

See Methods. ‘R-TH’ represents the Rooihoogte and Timeball Hill formations (this study). Prandom is the ‘false-positive’ probability that the two sample sets separated by each pivot-age arise from populations of the same mean and variance. As discussed in the text, this value reaches an extreme of −31 when the sample sets are split into the time periods 0.70–2.71 Gyr ago and 2.75–3.80 Gyr ago (not shown).

Extended Data Figure 2 Stratigraphic context for the Rooihoogte and Timeball Hill formations within the Eastern Transvaal basin, South Africa, and associated ages.

‘MIF’ is the disappearance of the mass-independent fractionation of sulfur isotopes in the underlying Duitschland Formation (now known to reappear in the Rooihoogte Formation6). Fm, formation. Image adapted from ref. 5, Elsevier.

Extended Data Figure 3 Simplified geologic map of the Transvaal Supergroup outcrop area.

The location of drill core EBA-2 is shown. The core is currently stored at the National Core Library at Donkerhoek, which is managed by the Council for Geoscience in South Africa. Gp, group. Image adapted from ref. 43, Geological Society of South Africa.

Extended Data Figure 4 Additional data for kerogen analyses.

a, Kerogen δ15N (δ15Norg, in ‰) versus kerogen N abundance (% Norg). b, δ15Norg versus organic δ13C (δ13Corg, in ‰). c, Total organic carbon (% TOC) versus organic δ13C. For all data points, errors are within the size of the symbols.

Source data

Extended Data Figure 5 Additional data for bulk-rock analyses.

a, Bulk-rock δ15N (δ15Nbulk, in ‰) versus total nitrogen (% TN). b, δ15Nbulk versus TOC:TN atomic ratios. c, % TN versus K2O content (%). d, δ15Nbulk versus K2O content. For all data points, errors are within the size of the symbols.

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Zerkle, A., Poulton, S., Newton, R. et al. Onset of the aerobic nitrogen cycle during the Great Oxidation Event. Nature 542, 465–467 (2017). https://doi.org/10.1038/nature20826

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