Mid-Proterozoic redox evolution and the possibility of transient oxygenation events
Abstract
It is often assumed that rising environmental oxygen concentrations played a significant role in the timing of the first appearance of animals and the trajectory of their early proliferation and diversification. The inherent large size and complexity of animals come with large energy requirements — levels of energy that can best, if not only, be acquired through aerobic respiration. There is also abundant geochemical evidence for an increase in ocean–atmosphere O2 concentrations in temporal proximity with the emergence of the group. To adequately test this hypothesis, however, a thorough understanding of the history of environmental oxygenation in the time between the first appearance of eukaryotes and the eventual appearance of animals is necessary. In this review, we summarize the evidence for the prevailing long-term conditions of the Proterozoic Eon prior to the emergence of Metazoa and go on to highlight multiple independent geochemical proxy records that suggest at least two transient oxygenation events — at ca. 1.4 and ca. 1.1 billion years ago (Ga) — during this time. These emerging datasets open the door to an important possibility: while prevailing conditions during much of this time would likely have presented challenges for early animals, there were intervals when oxygenated conditions were more widespread and could have favored yet undetermined advances in eukaryotic innovation, including critical early steps toward animal evolution.
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Tectonic models related to rifting during breakup of the Nuna supercontinent at ∼1.4 Ga could provide a mechanism for periods of enhanced organic burial and related transient oxygenation.
“Tectonic models during this interval as specifically related to rifting during breakup of the Nuna supercontinent at ∼1.4 Ga could provide a mechanism for periods of enhanced organic burial and related transient oxygenation (Zhang et al., 2012; Canfield et al., 2018; Diamond and Lyons, 2018; Large et al., 2019; Steadman et al., 2020).”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Diamond and Lyons, 2018
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Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview
Lyons, T. W., Diamond, C. W., Planavsky, N. J., Reinhard, C. T., & Li, C. (2021) · Astrobiology · doi:10.1089/ast.2020.2418 · Cited by 211 · see citing works
“4 Ga could provide a mechanism for periods of enhanced organic burial and related transient oxygenation (Zhang et al., 2012; Canfield et al., 2018; Diamond and Lyons, 2018; Large et al., 2019; Steadman et al., 2020).”
BackgroundInfluentialSelf-citationSedimentary Ce anomalies: Secular change and implications for paleoenvironmental evolution
Zhang, K., & Shields, G. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.104015 · Cited by 160 · see citing works
On the co‐evolution of surface oxygen levels and animals
Cole, D. B., Mills, D. B., Erwin, D. H., Sperling, E. A., Porter, S. M., Reinhard, C. T., & Planavsky, N. J. (2020) · Geobiology · doi:10.1111/gbi.12382 · Cited by 141 · see citing works
Breathless through Time: Oxygen and Animals across Earth’s History
Sperling, E. A., Boag, T. H., Duncan, M. I., Endriga, C. R., Marquez, J. A., Mills, D. B., Monarrez, P. M., Sclafani, J. A., Stockey, R., & Payne, J. L. (2022) · Biological Bulletin · doi:10.1086/721754 · Cited by 87 · see citing works
Reconstructing Earth’s atmospheric oxygenation history using machine learning
Chen, G.-X., Cheng, Q., Lyons, T., Shen, J., Agterberg, F., Huang, N., & Zhao, M. (2022) · Nature Communications · doi:10.1038/s41467-022-33388-5 · Cited by 64 · see citing works
Self-citationCOHEN, P. A., & Kodner, R. B. (2021) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2021.11.005 · Cited by 65 · see citing works
A transient swing to higher oxygen levels in the atmosphere and oceans at ~1.4 Ga
Wei, W., Frei, R., Klaebe, R., Tang, D., Wei, G., Li, D., Tian, L., Huang, F., & Ling, H. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.106058 · Cited by 52 · see citing works
Antimicrobial Activity of Metals and Metalloids
Li, Y. P., Fekih, I. B., Fru, E. C., Moraleda‐Muñoz, A., Li, X., Rosen, B. P., Yoshinaga, M., & Rensing, C. (2021) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032921-123231 · Cited by 50 · see citing works
Evidence for elevated and variable atmospheric oxygen in the Precambrian
Steadman, J. A., Large, R. R., Blamey, N. J., Mukherjee, I., Corkrey, R., Danyushevsky, L. V., Maslennikov, V., Hollings, P., Garven, G., Brand, U., et al. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.105722 · Cited by 47 · see citing works
Weathering, alteration and reconstructing Earth's oxygenation
Planavsky, N. J., Robbins, L. J., Kamber, B. S., & Schoenberg, R. (2020) · Interface Focus · doi:10.1098/rsfs.2019.0140 · Cited by 45 · see citing works
A very unconventional hydrocarbon play: The Mesoproterozoic Velkerri Formation of northern Australia
Cox, G. M., Collins, A. S., Jarrett, A. J. M., Blades, M., Shannon, A., Yang, B., Farkaš, J., Hall, T., O’Hara, B., Close, D., et al. (2022) · AAPG Bulletin · doi:10.1306/12162120148 · Cited by 44 · see citing works
Evolution of the crustal phosphorus reservoir
Walton, C. R., Hao, J., Huang, F., Jenner, F. E., Williams, H. M., Zerkle, A. L., Lipp, A., Hazen, R. M., Peters, S. E., & Shorttle, O. (2023) · Science Advances · doi:10.1126/sciadv.ade6923 · Cited by 40 · see citing works
Hao, F., Tang, D., Shi, X., Lechte, M. A., Shang, M., Zhou, X., & Yu, W. (2020) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2020.109966 · Cited by 38 · see citing works
Colwyn, D. A., Sheldon, N. D., Maynard, J. B., Gaines, R. R., Hofmann, A., Wang, X., Guéguen, B., Asael, D., Reinhard, C. T., & Planavsky, N. J. (2019) · Geobiology · doi:10.1111/gbi.12360 · Cited by 36 · see citing works
Gilleaudeau, G. J., Sahoo, S., Ostrander, C. M., Owens, J. D., Poulton, S. W., Lyons, T. W., & Anbar, A. D. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.105718 · Cited by 34 · see citing works
Self-citationOrganic matter sulfurization and organic carbon burial in the Mesoproterozoic
Raven, M. R., Crockford, P. W., Hodgskiss, M. S. W., Lyons, T. W., Tino, C., & Webb, S. M. (2023) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2023.02.020 · Cited by 32 · see citing works
Self-citationSpinks, S., Sperling, E. A., Thorne, R. L., LaFountain, F., White, A. J. R., Armstrong, J., Woltering, M., & Tyler, I. (2022) · Geobiology · doi:10.1111/gbi.12524 · Cited by 28 · see citing works
Wei, B., Tang, D., Shi, X., Lechte, M. A., Zhou, L., Zhou, X., & Song, H. (2021) · Geochemistry Geophysics Geosystems · doi:10.1029/2020gc009612 · Cited by 28 · see citing works
The Pyrite Trace Element Paleo-Ocean Chemistry Proxy
Gregory, D. D. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108846974 · Cited by 26 · see citing works
Sedimentary pyrite proxy for atmospheric oxygen; evaluation of strengths and limitations
Large, R., Mukherjee, I., Danyushevsky, L., Gregory, D., Steadman, J., & Corkrey, R. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.103941 · Cited by 23 · see citing works
Diamond, C. W., Ernst, R. E., Zhang, S., & Lyons, T. W. (2021) · Geophysical Monograph Series · doi:10.1002/9781119507444.ch21 · Cited by 25 · see citing works
Self-citationUranium isotope cycling on the highly productive Peruvian margin
Bruggmann, S., Gilleaudeau, G. J., Romaniello, S. J., Severmann, S., Canfield, D. E., Anbar, A. D., Scholz, F., & Frei, R. (2021) · Chemical Geology · doi:10.1016/j.chemgeo.2021.120705 · Cited by 25 · see citing works
Shi, Q., Shi, X., Tang, D., Fan, C., Wei, B., & Li, Y. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.106050 · Cited by 22 · see citing works
Transient deep-water oxygenation recorded by rare Mesoproterozoic phosphorites, South Urals
Stüeken, E., Kuznetsov, A. B., Vasilyeva, I. M., Krupenin, M., & Bekker, A. (2021) · Precambrian Research · doi:10.1016/j.precamres.2021.106242 · Cited by 22 · see citing works
Li, Z., Cole, D. B., Newby, S. M., Owens, J. D., Kendall, B., & Reinhard, C. T. (2021) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2021.09.006 · Cited by 18 · see citing works
Xu, L., Lechte, M. A., Shi, X., Zheng, W., Zhou, L., Huang, K., Zhou, X., & Tang, D. (2024) · Geophysical Research Letters · doi:10.1029/2023gl106654 · Cited by 16 · see citing works
Cornet, Y., François, C., Compère, P., Callec, Y., Roberty, S., Plumier, J.-C., & Javaux, E. (2019) · Precambrian Research · doi:10.1016/j.precamres.2019.105410 · Cited by 16 · see citing works
Large Igneous Provinces (LIPs) and Anoxia Events in “The Boring Billion”
Zhang, S., Ernst, R. E., Pei, J., Zhao, Y. J., & Hu, G. (2021) · Geophysical monograph · doi:10.1002/9781119507444.ch20 · Cited by 15 · see citing works
Eguchi, J., Diamond, C., & Lyons, T. W. (2022) · PNAS Nexus · doi:10.1093/pnasnexus/pgac036 · Cited by 14 · see citing works
Self-citationOn the use of models in understanding the rise of complex life
Lenton, T. M. (2020) · Interface Focus · doi:10.1098/rsfs.2020.0018 · Cited by 12 · see citing works
Global tectonics and oxygenation events drove the Earth-scale phosphorus cycle
Ma, C., Tang, Y., & Ying, J. (2022) · Earth-Science Reviews · doi:10.1016/j.earscirev.2022.104166 · Cited by 12 · see citing works
Ning, G., Wei, J., Yueer, L., & Yu, K. (2025) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2025.113082 · Cited by 10 · see citing works
Application of Cd as a paleo-environment indicator
Ye, Y., Wang, H., Wang, X., Wu, C., Canfield, D. E., & Zhang, S. (2021) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2021.110749 · Cited by 11 · see citing works
Fuchsman, C. A., & Stüeken, E. E. (2020) · Environmental Microbiology · doi:10.1111/1462-2920.15220 · Cited by 9 · see citing works
Yan, H., Xu, L., Mao, J., Tang, D., Yang, X., Bai, Y., Li, C., Konhauser, K. O., & Robbins, L. J. (2023) · American Mineralogist · doi:10.2138/am-2022-8919 · Cited by 7 · see citing works
Ma, P., Guo, H., Du, Y., Yu, W., Jin, S., & Xu, L. (2023) · Precambrian Research · doi:10.1016/j.precamres.2022.106953 · Cited by 7 · see citing works
An expansive global oxygenation of Earth’s surface environments 1.4 billion years ago
Yan, H., Qin, Z., Xu, L., Jingwen, M., Tang, D., Huang, Q., Yang, X., Li, Z., Li, J., Li, L., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65551-z · Cited by 7 · see citing works
Early Earth and the rise of complex life
Lyons, T. W., Droser, M. L., Lau, K., & Porter, S. M. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20180093 · Cited by 5 · see citing works
Self-citationEvolution of Earth's Atmosphere
Large, R. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-409548-9.11853-6 · Cited by 5 · see citing works
Johnson, C. M., Beard, B. L., & Weyer, S. (2020) · Advances in isotope geochemistry · doi:10.1007/978-3-030-33828-2_6 · Cited by 4 · see citing works
Park, J. G., Hudgins, M., Fralick, P. W., Shelley, J. T., & Schaller, M. F. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2513030122 · Cited by 3 · see citing works
Oxygenation of the Proterozoic Earth's surface: An evolving story
Kendall, B., & Ostrander, C. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99762-1.00058-9 · Cited by 3 · see citing works
Zhang, C., Tian, W., He, Y., Gong, M., & Li, S. (2024) · Frontiers in Earth Science · doi:10.3389/feart.2024.1368342 · Cited by 2 · see citing works
Ocean redox evolution past and present
Hardisty, D. S., & Lau, K. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99762-1.00033-4 · Cited by 2 · see citing works
Gilleaudeau, G. J., Sahoo, S., Ostrander, C. M., Owens, J. D., Poulton, S. W., Lyons, T. W., & Anbar, A. D. (2019) · Abstracts with programs - Geological Society of America · doi:10.1130/abs/2019am-339003
Self-citationThe nature of the rock record: Through the lens of the rock cycle
Walton, C. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99762-1.00120-0
Ghnahalla, M., Rouxel, O. J., Fru, E. C., Bankole, O. M., Sabar, M. S., Elmola, A. A., Chraiki, I., Abdelfadel, F., Fontaine, C., Trentesaux, A., et al. (2024) · Gondwana Research · doi:10.1016/j.gr.2024.08.012
- Authors
- Diamond, C. W., & Lyons, T. W.
- Affiliations
- University of California, Riverside (US)
- Corresponding author
- Diamond, Charles W.
- Venue
- Emerging Topics in Life Sciences
- Publisher
- Portland Press Ltd.
- Published
- 2018-07-13
- Volume
- 2
- Issue
- 2
- Pages
- 235-245
- ISSN
- 2397-8554 (ISSN-L)
- 2397-8562
- OpenAlex
- W2883969747
- Cited by
- 49
- References
- 92
- Citations by year
- 2025: 3 · 2024: 7 · 2023: 4 · 2022: 9 · 2021: 10 · 2020: 11 · 2019: 4 · 2018: 1
- FWCI
- 4.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Emerging Topics in Life Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- NASA Astrobiology Institute
- Science Mission Directorate
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- early animal evolution, Ediacaran, Neoproterozoic, ocean oxygenation, eukaryotic evolution, geochemical proxies, aerobic respiration, origin of animals
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