Advertisement

Stepping to an internal beat

What caused the stepwise nature of the rise of molecular oxygen in Earth's atmosphere since it appeared in large quantities more than 2 billion years ago? Alcott et al. argue that a set of internal feedbacks involving the global phosphorus, carbon, and oxygen cycles, not individual external forces, could be responsible. Their model, which depends only on a gradual shift from reducing to oxidizing surface conditions over time, produces the same three-step pattern observed in the geological record.
Science, this issue p. 1333

Abstract

Oxygenation of Earth’s atmosphere and oceans occurred across three major steps during the Paleoproterozoic, Neoproterozoic, and Paleozoic eras, with each increase having profound consequences for the biosphere. Biological or tectonic revolutions have been proposed to explain each of these stepwise increases in oxygen, but the principal driver of each event remains unclear. Here we show, using a theoretical model, that the observed oxygenation steps are a simple consequence of internal feedbacks in the long-term biogeochemical cycles of carbon, oxygen, and phosphorus, and that there is no requirement for a specific stepwise external forcing to explain the course of Earth surface oxygenation. We conclude that Earth’s oxygenation events are entirely consistent with gradual oxygenation of the planetary surface after the evolution of oxygenic photosynthesis.
Get full access to this article

View all available purchase options and get full access to this article.

Already a Subscriber?

Supplementary Material

Summary

Materials and Methods
Supplementary Text
Figs. S1 to S4
Tables S1 to S3
References (4852)

Resources

File (aax6459_alcott_sm.pdf)
File (pap.pdf)

References and Notes

1
J. Farquhar, H. Bao, M. Thiemens, Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–759 (2000).
2
N. J. Planavsky, C. T. Reinhard, X. Wang, D. Thomson, P. McGoldrick, R. H. Rainbird, T. Johnson, W. W. Fischer, T. W. Lyons, Earth history. Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638 (2014).
3
D. S. Hardisty, Z. Lu, A. Bekker, C. W. Diamond, B. C. Gill, G. Jiang, L. C. Kah, A. H. Knoll, S. J. Loyd, M. R. Osburn, N. J. Planavsky, C. Wang, X. Zhou, T. W. Lyons, Perspectives on Proterozoic surface ocean redox from iodine contents in ancient and recent carbonate. Earth Planet. Sci. Lett. 463, 159–170 (2017).
4
S. W. Poulton, D. E. Canfield, Ferruginous Conditions: A Dominant Feature of the Ocean through Earth’s History. Elements 7, 107–112 (2011).
5
L. Och, G. Shields-Zhou, The Neoproterozoic oxygenation event: Environmental pertubations and biogeochemical cycling. Earth Sci. Rev. 110, 26–57 (2012).
6
S. K. Sahoo, N. J. Planavsky, G. Jiang, B. Kendall, J. D. Owens, X. Wang, X. Shi, A. D. Anbar, T. W. Lyons, Oceanic oxygenation events in the anoxic Ediacaran ocean. Geobiology 14, 457–468 (2016).
7
A. J. Krause, B. J. W. Mills, S. Zhang, N. J. Planavsky, T. M. Lenton, S. W. Poulton, Stepwise oxygenation of the Paleozoic atmosphere. Nat. Commun. 9, 4081 (2018).
8
N. J. Butterfield, Early evolution of the Eukaryota. Palaeontology 58, 5–17 (2015).
9
J. J. Brocks, A. J. M. Jarrett, E. Sirantoine, C. Hallmann, Y. Hoshino, T. Liyanage, The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017).
10
K. M. Meyer, A. Ridgwell, J. L. Payne, The influence of the biological pump on ocean chemistry: Implications for long-term trends in marine redox chemistry, the global carbon cycle, and marine animal ecosystems. Geobiology 14, 207–219 (2016).
11
T. M. Lenton, R. A. Boyle, S. W. Poulton, G. A. Shields-Zhou, N. J. Butterfield, Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).
12
L. R. Kump, M. E. Barley, Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448, 1033–1036 (2007).
13
C.-T. A. Lee, L. Y. Yeung, N. R. McKenzie, Y. Yokoyama, K. Ozaki, A. Lenardic, Two-step rise of atmospheric oxygen linked to the growth of continents. Nat. Geosci. 9, 417–424 (2016).
14
I. H. Campbell, C. M. Allen, Formation of supercontinents linked to increases in atmospheric oxygen. Nat. Geosci. 1, 554–558 (2008).
15
F. Horton, Did phosphorus derived from the weathering of large igneous provinces fertilize the Neoproterozoic ocean? Geochem. Geophys. Geosyst. 16, 1723–1738 (2015).
16
A. H. Knoll, M. A. Nowak, The timetable of evolution. Sci. Adv. 3, e1603076 (2017).
17
T. M. Lenton, S. J. Daines, The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic-Phanerozoic transition. Emerg. Top. Life Sci. 2, 267–278 (2018).
18
C. Goldblatt, T. M. Lenton, A. J. Watson, Bistability of atmospheric oxygen and the Great Oxidation. Nature 443, 683–686 (2006).
19
M. W. Claire, D. C. Catling, K. J. Zahnle, Biogeochemical modelling of the rise in atmospheric oxygen. Geobiology 4, 239–269 (2006).
20
T. A. Laakso, D. P. Schrag, A theory of atmospheric oxygen. Geobiology 15, 366–384 (2017).
21
T. A. Laakso, D. P. Schrag, Regulation of atmospheric oxygen during the Proterozoic. Earth Planet. Sci. Lett. 388, 81–91 (2014).
22
T. Tyrrell, The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400, 525–531 (1999).
23
M. D. Krom, R. A. Berner, The diagenesis of phosphorus in a nearshore marine sediment. Geochim. Cosmochim. Acta 45, 207–216 (1981).
24
K. C. Ruttenberg, R. A. Berner, Authigenic apatite formation and burial in sediments from non-upwelling, continental margin environments. Geochim. Cosmochim. Acta 57, 991–1007 (1993).
25
T. Jilbert, C. P. Slomp, Iron and manganese shuttles control the formation of authigenic phosphorus minerals in the euxinic basins of the Baltic Sea. Geochim. Cosmochim. Acta 107, 155–169 (2013).
26
P. Van Cappellen, E. D. Ingall, Benthic phosphorus regeneration, net primary production, and ocean anoxia: A model of the coupled marine biogeochemical cycles of carbon and phosphorus. Paleoceanography 9, 677–692 (1994).
27
C. P. Slomp, J. Thomson, G. J. De Lange, Enhanced regeneration of phosphorus during formation of the most recent eastern Mediterranean sapropel (S1). Geochim. Cosmochim. Acta 66, 1171–1184 (2002).
28
I. Tsandev, C. P. Slomp, Modelling phosphorus cycling and carbon burial during Cretaceous Oceanic Anoxic Events. Earth Planet. Sci. Lett. 286, 71–79 (2009).
29
C. T. Reinhard, N. J. Planavsky, B. C. Gill, K. Ozaki, L. J. Robbins, T. W. Lyons, W. W. Fischer, C. Wang, D. B. Cole, K. O. Konhauser, Evolution of the global phosphorus cycle. Nature 541, 386–389 (2017).
30
S. J. Daines, B. J. W. Mills, T. M. Lenton, Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon. Nat. Commun. 8, 14379 (2017).
31
I. C. Handoh, T. M. Lenton, Periodic mid-Cretaceous oceanic anoxic events linked by oscillations of the phosphorus and oxygen biogeochemical cycles. Global Biogeochem. Cycles 17, 1092 (2003).
32
C. P. Slomp, P. Van Cappellen, The global marine phosphorus cycle: Sensitivity to oceanic circulation. Biogeosciences 4, 155–171 (2007).
33
I. Tsandev, C. P. Slomp, P. Van Cappellen, Glacial-interglacial variations in marine phosphorus cycling: Implications for ocean productivity. Global Biogeochem. Cycles 22, GB4004 (2008).
34
P. Kharecha, J. F. Kasting, J. Siefert, A coupled atmosphere-ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005).
35
J. Krissansen-Totton, G. N. Arney, D. C. Catling, Constraining the climate and ocean pH of the early Earth with a geological carbon cycle model. Proc. Natl. Acad. Sci. U.S.A. 115, 4105–4110 (2018).
36
A. A. Pavlov, J. F. Kasting, Mass-independent fractionation of sulfur isotopes in Archean sediments: Strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27–41 (2002).
37
D. C. Catling, M. W. Claire, How Earth’s atmosphere evolved to an oxic state: A status report. Earth Planet. Sci. Lett. 237, 1–20 (2005).
38
E. A. Sperling, C. J. Wolock, A. S. Morgan, B. C. Gill, M. Kunzmann, G. P. Halverson, F. A. Macdonald, A. H. Knoll, D. T. Johnston, Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454 (2015).
39
K. Wallmann, Feedbacks between oceanic redox states and marine productivity: A model perspective focused on benthic phosphorus cycling. Global Biogeochem. Cycles 17, 1084 (2003).
40
W. S. Broecker, T. H. Peng, Tracers in the Sea (Eldigio Press, 1982).
41
C. J. Bjerrum, D. E. Canfield, T. W. Dahl, “Chasing Neoptoerozoic Atmospheric Oxygen Ghosts,” abstract PP21D-06, presented at the American Geophysical Union Fall Meeting 2016, San Francisco, CA, 12 to 16 December 2016.
42
T. M. Lenton, S. J. Daines, B. J. W. Mills, COPSE reloaded: An improved model of biogeochemical cycling over Phanerozoic time. Earth Sci. Rev. 178, 1–28 (2018).
43
J. M. Hayes, J. R. Waldbauer, The carbon cycle and associated redox processes through time. Philos. Trans. R. Soc. B 361, 931–950 (2006).
44
D. C. Catling, K. J. Zahnle, C. McKay, Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839–843 (2001).
45
G. A. Shields, B. J. W. Mills, Tectonic controls on the long-term carbon isotope mass balance. Proc. Natl. Acad. Sci. U.S.A. 114, 4318–4323 (2017).
46
B. Mills, T. M. Lenton, A. J. Watson, Proterozoic oxygen rise linked to shifting balance between seafloor and terrestrial weathering. Proc. Natl. Acad. Sci. U.S.A. 111, 9073–9078 (2014).
47
T. W. Lyons, C. T. Reinhard, N. J. Planavsky, The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).
48
K. C. Ruttenberg, Reassessment of the oceanic residence time of phosphorus. Chem. Geol. 107, 405–409 (1993).
49
A. J. Watson, T. M. Lenton, B. J. W. Mills, Ocean deoxygenation, the global phosphorus cycle and the possibility of human-caused large-scale ocean anoxia. Philos. Trans. R. Soc. A 375, 20160318 (2017).
50
E. D. Ingall, R. M. Bustin, P. Van Cappellen, Influence of water column anoxia on the burial and preservation of carbon and phosphorus in marine shales. Geochim. Cosmochim. Acta 57, 303–316 (1993).
51
S. W. Poulton, Early Phosphorus Redigested. Nat. Geosci. 10, 75–76 (2017).
52
N. M. Bergman, T. M. Lenton, A. J. Watson, COPSE: A new model of biogeochemical cycling over Phanerozoic time. Am. J. Sci. 304, 397–437 (2004).

Information & Authors

Information

Published In

Science
Volume 366Issue 647113 December 2019
Pages: 1333 - 1337
PubMed: 31826958

History

Received: 11 April 2019
Accepted: 17 October 2019
10 December 2019

Permissions

Request permissions for this article.

Acknowledgments

We thank C. Slomp and K. Wallmann for sending computer code; we also thank the reviewers of this work for constructive and useful comments. Funding: L.J.A. is funded by a Leeds Anniversary Research Scholarship. B.J.W.M. acknowledges support from a University of Leeds Academic Fellowship. S.W.P. acknowledges support from a Leverhulme Research Fellowship and a Royal Society Wolfson Research Merit Award. B.J.W.M. and S.W.P. are funded by the UK Natural Environment Research Council (NE/R010129/1 and NE/S009663/1). Author contributions: L.J.A. and B.J.W.M. designed the research and developed the model. L.J.A. performed model runs. All authors wrote the manuscript. Competing interests: The authors declare no competing interests. Data and materials availability: All data are available in the main text or the supplementary materials. Model code and output data are available from the corresponding author on request.

Authors

Affiliations

School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK.
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK.
School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK.

Notes

*Corresponding author. Email: [email protected]

Funding Information

Leeds Anniversary Research Scholarship:

Metrics & Citations

Metrics

Citations

View Options

Media

Figures

Other

Tables

Share

Information & Authors
Published In
issue cover image
Science
Volume 366|Issue 6471
13 December 2019
Article Versions
You are viewing the most recent version of this article.
Submission history
Received:11 April 2019
Accepted:17 October 2019
Published in print:13 December 2019
Metrics & Citations
Article Usage
Altmetrics
Export citation

Select the format you want to export the citation of this publication.

Cited by
  1. Photochemical modelling of atmospheric oxygen levels confirms two stable states, Earth and Planetary Science Letters, 561, (116818), (2021).https://doi.org/10.1016/j.epsl.2021.116818
    Crossref
  2. Global marine redox evolution from the late Neoproterozoic to the early Paleozoic constrained by the integration of Mo and U isotope records, Earth-Science Reviews, 214, (103506), (2021).https://doi.org/10.1016/j.earscirev.2021.103506
    Crossref
  3. Evolution of the structure and impact of Earth’s biosphere, Nature Reviews Earth & Environment, 2, 2, (123-139), (2021).https://doi.org/10.1038/s43017-020-00116-w
    Crossref
  4. Quantification and interpretation of the climate variability record, Global and Planetary Change, 197, (103399), (2021).https://doi.org/10.1016/j.gloplacha.2020.103399
    Crossref
  5. Recent Advances in Geochemical Paleo-Oxybarometers, Annual Review of Earth and Planetary Sciences, 49, 1, (399-433), (2021).https://doi.org/10.1146/annurev-earth-071520-051637
    Crossref
  6. A protease-mediated mechanism regulates the cytochrome c 6 /plastocyanin switch in Synechocystis sp. PCC 6803 , Proceedings of the National Academy of Sciences, 118, 5, (e2017898118), (2021).https://doi.org/10.1073/pnas.2017898118
    Crossref
  7. Heterogeneous redox evolution of the Meso-Neoproterozoic ocean: Insights from eastern China, Palaeogeography, Palaeoclimatology, Palaeoecology, 567, (110304), (2021).https://doi.org/10.1016/j.palaeo.2021.110304
    Crossref
  8. Possible link between Earth’s rotation rate and oxygenation, Nature Geoscience, 14, 8, (564-570), (2021).https://doi.org/10.1038/s41561-021-00784-3
    Crossref
  9. Carbon cycle inverse modeling suggests large changes in fractional organic burial are consistent with the carbon isotope record and may have contributed to the rise of oxygen, Geobiology, 19, 4, (342-363), (2021).https://doi.org/10.1111/gbi.12440
    Crossref
  10. The oxygen cycle and a habitable Earth, Science China Earth Sciences, 64, 4, (511-528), (2021).https://doi.org/10.1007/s11430-020-9747-1
    Crossref
  11. See more
Loading...
Share
Share article link

Share on social media
Get Access
Log in to view the full text

AAAS Log in

AAAS login provides access to Science for AAAS members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.
More options

Register for free to read this article

As a service to the community, this article is available for free. Login or register for free to read this article.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View Options
Tables
References

(0)eLetters

eLetters is an online forum for ongoing peer review. Submission of eLetters are open to all. eLetters are not edited, proofread, or indexed. Please read our Terms of Service before submitting your own eLetter.

No eLetters have been published for this article yet.