The rise of algae in Cryogenian oceans and the emergence of animals
Abstract
The transition from dominant bacterial to eukaryotic marine primary productivity was one of the most profound ecological revolutions in the Earth's history, reorganizing the distribution of carbon and nutrients in the water column and increasing energy flow to higher trophic levels. But the causes and geological timing of this transition, as well as possible links with rising atmospheric oxygen levels and the evolution of animals, remain obscure. Here we present a molecular fossil record of eukaryotic steroids demonstrating that bacteria were the only notable primary producers in the oceans before the Cryogenian period (720-635 million years ago). Increasing steroid diversity and abundance marks the rapid rise of marine planktonic algae (Archaeplastida) in the narrow time interval between the Sturtian and Marinoan 'snowball Earth' glaciations, 659-645 million years ago. We propose that the incumbency of cyanobacteria was broken by a surge of nutrients supplied by the Sturtian deglaciation. The 'Rise of Algae' created food webs with more efficient nutrient and energy transfers, driving ecosystems towards larger and increasingly complex organisms. This effect is recorded by the concomitant appearance of biomarkers for sponges and predatory rhizarians, and the subsequent radiation of eumetazoans in the Ediacaran period.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
There are claims for the earliest reliable organic biomarkers for ancient eukaryotes around 800 Ma.
“An equally intriguing possibility lies with claims for the earliest reliable organic biomarkers for ancient eukaryotes around 800 Ma (Brocks et al., 2016, 2017; Zumberge et al., 2020; and references cited therein)”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Brocks et al., 2017
The interglacial between the Sturtian and Marinoan glaciations is the same interval that produced the earliest records of animals (sponges) and diversification among eukaryotes more generally, including emergence of the earliest predatory rhizarians.
“The interglacial is the same interval that produced the earliest records of animals (sponges; Love et al., 2009; Love and Summons, 2015), as well as diversification among eukaryotes more generally, including emergence of the earliest predatory rhizarians (Brocks et al., 2017)—a group that includes radiolaria and foraminifera.”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Brocks et al., 2017
Recent organic geochemical data suggest that bacteria continued to dominate primary production until the interglacial between the Sturtian and Marinoan glaciations starting at roughly 660 Ma, while other data indicate a proliferation of eukaryotes starting closer to 800-750 Ma.
“Some recent organic geochemical data suggest that bacteria continued to dominate primary production until the interglacial between the Sturtian and Marinoan glaciations (Brocks et al., 2017) starting at roughly 660 Ma, while other data indicate a proliferation of eukaryotes starting closer to 800–750 Ma (Brocks et al., 2017; Brocks, 2018; Isson et al., 2018).”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Brocks et al., 2017
Cites
The rise of oxygen in Earth's early ocean and atmosphere
Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014) · Nature · doi:10.1038/nature13068 · Cited by 2,810 · see citing works
A Neoproterozoic Snowball Earth
Hoffman, P. F., Kaufman, A. J., Halverson, G. P., & Schrag, D. P. (1998) · Science · doi:10.1126/science.281.5381.1342 · Cited by 2,693 · see citing works
THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels
Canfield, D. E. (2005) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.33.092203.122711 · Cited by 1,032 · see citing works
Lethally Hot Temperatures During the Early Triassic Greenhouse
Sun, Y.-D., Joachimski, M., Wignall, P., Yan, C.-B., Chen, Y.-L., Jiang, H.-S., Wang, L., & Lai, X. (2012) · Science · doi:10.1126/science.1224126 · Cited by 980 · see citing works
Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes
Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A., & Keeling, P. J. (2015) · Science · doi:10.1126/science.1257594 · Cited by 930 · see citing works
Fossil steroids record the appearance of Demospongiae during the Cryogenian period
Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., Kelly, A. E., Bhatia, M., Meredith, W., Snape, C. E., et al. (2009) · Nature · doi:10.1038/nature07673 · Cited by 731 · see citing works
Evolution of the global phosphorus cycle
Reinhard, C. T., Planavsky, N. J., Gill, B. C., Ozaki, K., Robbins, L. J., Lyons, T. W., Fischer, W. W., Wang, C., Cole, D. B., & Konhauser, K. O. (2017) · Nature · doi:10.1038/nature20772 · Cited by 649 · see citing works
Grantham, P. J., & Wakefield, L. L. (1988) · Organic Geochemistry · doi:10.1016/0146-6380(88)90115-5 · Cited by 549 · see citing works
The evolution of the marine phosphate reservoir
Planavsky, N. J., Rouxel, O. J., Bekker, A., Lalonde, S. V., Konhauser, K. O., Reinhard, C. T., & Lyons, T. W. (2010) · Nature · doi:10.1038/nature09485 · Cited by 488 · see citing works
Scaling-up from nutrient physiology to the size-structure of phytoplankton communities
Irwin, A. J., Finkel, Z. V., Schofield, O., & Falkowski, P. G. (2006) · Journal of Plankton Research · doi:10.1093/plankt/fbi148 · Cited by 363 · see citing works
Pu, J. P., Bowring, S. A., Ramezani, J., Myrow, P., Raub, T. D., Landing, E., Mills, A., Hodgin, E., & Macdonald, F. A. (2016) · Geology · doi:10.1130/g38284.1 · Cited by 357 · see citing works
Oceanic oxygenation events in the anoxic Ediacaran ocean
Sahoo, S. K., Planavsky, N. J., Jiang, G., Kendall, B., Owens, J. D., Wang, X., Shi, X., Anbar, A. D., & Lyons, T. W. (2016) · Geobiology · doi:10.1111/gbi.12182 · Cited by 352 · see citing works
Reappraisal of hydrocarbon biomarkers in Archean rocks
French, K. L., Hallmann, C., Hope, J. M., Schoon, P. L., Zumberge, J. A., Hoshino, Y., Peters, C. A., George, S. C., Love, G. D., Brocks, J. J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419563112 · Cited by 307 · see citing works
Self-citationEarly photosynthetic eukaryotes inhabited low-salinity habitats
Sánchez-Baracaldo, P., Raven, J., Pisani, D., & Knoll, A. (2017) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1620089114 · Cited by 294 · see citing works
Continental flood basalt weathering as a trigger for Neoproterozoic Snowball Earth
Cox, G. M., Halverson, G. P., Stevenson, R. K., Vokaty, M., Poirier, A., Kunzmann, M., Li, Z., Denyszyn, S. W., Strauss, J. V., & Macdonald, F. A. (2016) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2016.04.016 · Cited by 282 · see citing works
Proterozoic and early Cambrian protists: evidence for accelerating evolutionary tempo.
Knoll, A. H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.6743 · Cited by 264 · see citing works
The Geological Succession of Primary Producers in the Oceans
KNOLL, A. H., SUMMONS, R. E., WALDBAUER, J. R., & ZUMBERGE, J. E. (2007) · Evolution of Primary Producers in the Sea · doi:10.1016/b978-012370518-1/50009-6 · Cited by 249 · see citing works
Kodner, R. B., Pearson, A., Summons, R. E., & Knoll, A. H. (2008) · Geobiology · doi:10.1111/j.1472-4669.2008.00167.x · Cited by 229 · see citing works
Origin of petroleum in the Neoproterozoic–Cambrian South Oman Salt Basin
Grosjean, E., Love, G. D., Stalvies, C., Fike, D. A., & Summons, R. E. (2008) · Organic Geochemistry · doi:10.1016/j.orggeochem.2008.09.011 · Cited by 222 · see citing works
Sterane biomarkers as indicators of palaeozoic algal evolution and extinction events
Schwark, L., & Empt, P. (2006) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2006.03.050 · Cited by 212 · see citing works
Summons, R. E., Brassell, S. C., Eglinton, G., Evans, E., Horodyski, R. J., Robinson, N., & Ward, D. M. (1988) · Geochimica et Cosmochimica Acta · doi:10.1016/0016-7037(88)90031-2 · Cited by 205 · see citing works
Krissansen-Totton, J., Buick, R., & Catling, D. C. (2015) · American Journal of Science · doi:10.2475/04.2015.01 · Cited by 180 · see citing works
Photosynthetic activities of a thermophilic blue-green alga
Yamaoka, T., Satoh, K., & Katoh, S. (1978) · Plant and Cell Physiology · doi:10.1093/oxfordjournals.pcp.a075684 · Cited by 176 · see citing works
The Proterozoic Record of Eukaryotes
Cohen, P. A., & Macdonald, F. A. (2015) · Paleobiology · doi:10.1017/pab.2015.25 · Cited by 173 · see citing works
Regulation of atmospheric oxygen during the Proterozoic
Laakso, T. A., & Schrag, D. P. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.11.049 · Cited by 159 · see citing works
Causes and consequences of mid-Proterozoic anoxia: CAUSES OF MID-PROTEROZOIC ANOXIA
Derry, L. A. (2015) · Geophysical Research Letters · doi:10.1002/2015gl065333 · Cited by 147 · see citing works
Brocks, J. J., Grosjean, E., & Logan, G. A. (2008) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2007.11.028 · Cited by 143 · see citing works
Self-citationThe survival of benthic macroscopic phototrophs on a Neoproterozoic snowball Earth
Ye, Q., Tong, J., Xiao, S., Zhu, S., An, Z., Tian, L., & Hu, J. (2015) · Geology · doi:10.1130/g36640.1 · Cited by 118 · see citing works
Brocks, J. J. (2011) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2011.03.014 · Cited by 117 · see citing works
Self-citationProterozoic photosynthesis – a critical review
Butterfield, N. J. F. (2015) · Palaeontology · doi:10.1111/pala.12211 · Cited by 116 · see citing works
Selenium isotope evidence for progressive oxidation of the Neoproterozoic biosphere
Pogge von Strandmann, P. A. E., Stüeken, E. E., Elliott, T., Poulton, S. W., Dehler, C. M., Canfield, D. E., & Catling, D. C. (2015) · Nature Communications · doi:10.1038/ncomms10157 · Cited by 111 · see citing works
Brocks, J. J., Jarrett, A. J. M., Sirantoine, E., Kenig, F., Moczydłowska, M., Porter, S., & Hope, J. (2016) · Geobiology · doi:10.1111/gbi.12165 · Cited by 109 · see citing works
Self-citationTiming of Neoproterozoic glaciations linked to transport-limited global weathering
Mills, B. J. W., Watson, A. J., Goldblatt, C., Boyle, R. A., & Lenton, T. M. (2011) · Nature Geoscience · doi:10.1038/ngeo1305 · Cited by 98 · see citing works
Persistence of a freshwater surface ocean after a snowball Earth
Yang, J., Jansen, M. F., Macdonald, F. A., & Abbot, D. S. (2017) · Geology · doi:10.1130/g38920.1 · Cited by 87 · see citing works
A bottom-up perspective on ecosystem change in Mesozoic oceans
Knoll, A. H., & Follows, M. J. (2016) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.1755 · Cited by 85 · see citing works
Eukaryotic Organisms in Extreme Acidic Environments, the Río Tinto Case
Aguilera, Á. (2013) · Life · doi:10.3390/life3030363 · Cited by 75 · see citing works
Riedman, L. A., Porter, S. M., Halverson, G. P., Hurtgen, M. T., & Junium, C. K. (2014) · Geology · doi:10.1130/g35901.1 · Cited by 62 · see citing works
Jarrett, A. J. M., Schinteie, R., Hope, J. M., & Brocks, J. J. (2013) · Organic Geochemistry · doi:10.1016/j.orggeochem.2013.06.005 · Cited by 48 · see citing works
Self-citationButterfield, N. J. (2009) · Geological Society, London, Special Publications · doi:10.1144/sp326.3 · Cited by 39 · see citing works
Brocks, J. J., & Hope, J. M. (2013) · Journal of Chromatographic Science · doi:10.1093/chromsci/bmt068 · Cited by 38 · see citing works
Self-citationSchinteie, R., & Brocks, J. J. (2014) · Organic Geochemistry · doi:10.1016/j.orggeochem.2014.04.009 · Cited by 31 · see citing works
Self-citationIdentification of 24-n-propylidenecholesterol in a member of the Foraminifera
Grabenstatter, J., Méhay, S., McIntyre-Wressnig, A., Giner, J., Edgcomb, V. P., Beaudoin, D., Bernhard, J. M., & Summons, R. E. (2013) · Organic Geochemistry · doi:10.1016/j.orggeochem.2013.08.010 · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Integrated records of environmental change and evolution challenge the Cambrian Explosion
Wood, R., Liu, A. G., Bowyer, F., Wilby, P. R., Dunn, F. S., Kenchington, C. G., Cuthill, J. F. H., Mitchell, E. G., & Penny, A. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0821-6 · Cited by 337 · see citing works
Strassert, J. F. H., Irisarri, I., Williams, T. A., & Burki, F. (2021) · Nature Communications · doi:10.1038/s41467-021-22044-z · Cited by 298 · see citing works
On the origin of oxygenic photosynthesis and Cyanobacteria
Sánchez‐Baracaldo, P., & Cardona, T. (2019) · New Phytologist · doi:10.1111/nph.16249 · Cited by 291 · see citing works
Cyanobacteria and biogeochemical cycles through Earth history
Sánchez-Baracaldo, P., Bianchini, G., Wilson, J. D., & Knoll, A. H. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.05.008 · Cited by 279 · see citing works
Diversity and ecology of protists revealed by metabarcoding
Burki, F., Sandín, M. M., & Jamy, M. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.066 · Cited by 247 · see citing works
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
“…organic biomarker evidence for eukaryotic life (steranes), when vetted for miscues linked to contamination, does not appear until *820 Ma (Brocks et al., 2017; Brocks, 2018; Zumberge et al., 2020)—despite many searches in diverse paleoenvironmental settings for earlier occurrences (e.g.,…”
BackgroundInfluentialTriple oxygen isotope evidence for limited mid-Proterozoic primary productivity
Crockford, P. W., Hayles, J. A., Bao, H., Planavsky, N. J., Bekker, A., Fralick, P. W., Halverson, G. P., Bui, T. H., Peng, Y., & Wing, B. A. (2018) · Nature · doi:10.1038/s41586-018-0349-y · Cited by 196 · see citing works
A one-billion-year-old multicellular chlorophyte
Tang, Q., Pang, K., Yuan, X., & Xiao, S. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1122-9 · Cited by 186 · see citing works
Biosilicification Drives a Decline of Dissolved Si in the Oceans through Geologic Time
Conley, D. J., Frings, P. J., Fontorbe, G., Clymans, W., Stadmark, J., Hendry, K., Marron, A. O., & Rocha, C. L. D. L. (2017) · Frontiers in Marine Science · doi:10.3389/fmars.2017.00397 · Cited by 177 · see citing works
Claypool continued: Extending the isotopic record of sedimentary sulfate
Crockford, P. W., Kunzmann, M., Bekker, A., Hayles, J. A., Bao, H., Halverson, G. P., Peng, Y., Bui, T. C. N., Cox, G. M., Gibson, T. M., et al. (2019) · Chemical Geology · doi:10.1016/j.chemgeo.2019.02.030 · Cited by 166 · see citing works
Dahl, T. W., & Arens, S. K. M. (2020) · Chemical Geology · doi:10.1016/j.chemgeo.2020.119665 · Cited by 160 · see citing works
Javaux, E. J., & Lepot, K. (2018) · Earth-Science Reviews · doi:10.1016/j.earscirev.2017.10.001 · Cited by 158 · see citing works
Rixen, T., Cowie, G., Gaye, B., Goés, J. I., Gomes, H. D. R., Hood, R. R., Lachkar, Z., Schmidt, H., Segschneider, J., & Singh, A. (2020) · Biogeosciences · doi:10.5194/bg-17-6051-2020 · Cited by 163 · see citing works
The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages
Fournier, G. P., Moore, K. R., Rangel, L. T., Payette, J. G., Momper, L., & Bosak, T. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0675 · Cited by 156 · see citing works
Sedimentary 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
Eukaryogenesis and oxygen in Earth history
Mills, D. B., Boyle, R. A., Daines, S. J., Sperling, E. A., Pisani, D., Donoghue, P. C. J., & Lenton, T. M. (2022) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01733-y · Cited by 153 · see citing works
Stepwise Earth oxygenation is an inherent property of global biogeochemical cycling
Alcott, L. J., Mills, B. J. W., & Poulton, S. W. (2019) · Science · doi:10.1126/science.aax6459 · Cited by 152 · see citing works
Coupling of ocean redox and animal evolution during the Ediacaran-Cambrian transition
Wang, D., Ling, H.-F., Struck, U., Zhu, X.-K., Zhu, M., He, T., Yang, B., Gamper, A., & Shields, G. A. (2018) · Nature Communications · doi:10.1038/s41467-018-04980-5 · Cited by 145 · 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
Lost world of complex life and the late rise of the eukaryotic crown
Brocks, J. J., Nettersheim, B. J., Adam, P., Schaeffer, P., Jarrett, A. J. M., Güneli, N., Liyanage, T., van Maldegem, L. M., Hallmann, C., & Hope, J. M. (2023) · Nature · doi:10.1038/s41586-023-06170-w · Cited by 135 · see citing works
Self-citationNeoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds
Cortona, A. D., Jackson, C. J., Bucchini, F., Bel, M. V., D’hondt, S., Škaloud, P., Delwiche, C. F., Knoll, A. H., Raven, J. A., Verbruggen, H., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910060117 · Cited by 133 · see citing works
Sperling, E. A., & Stockey, R. G. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy088 · Cited by 122 · see citing works
Wei, G.-Y., Planavsky, N. J., He, T., Zhang, F., Stockey, R. G., Cole, D. B., Lin, Y.-B., & Ling, H.-F. (2021) · Earth-Science Reviews · doi:10.1016/j.earscirev.2021.103506 · Cited by 122 · see citing works
Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals
Zumberge, J. A., Love, G. D., Cárdenas, P., Sperling, E. A., Gunasekera, S., Rohrssen, M., Grosjean, E., Grotzinger, J. P., & Summons, R. E. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0676-2 · Cited by 121 · see citing works
Lipid biomarkers: molecular tools for illuminating the history of microbial life
Summons, R. E., Welander, P. V., & Gold, D. A. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00636-2 · Cited by 115 · see citing works
Chen, Z., Tu, C., Pei, Y., Ogg, J. G., Fang, Y., Wu, S., Feng, X., Huang, Y., Guo, Z., & Yang, H. (2019) · Earth-Science Reviews · doi:10.1016/j.earscirev.2019.01.015 · Cited by 111 · see citing works
Gueneli, N., Mckenna, A. M., Ohkouchi, N., Boreham, C. J., Beghin, J., Javaux, E., & Brocks, J. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803866115 · Cited by 104 · see citing works
Self-citationGenomic and fossil windows into the secret lives of the most ancient fungi
Berbee, M. L., Strullu‐Derrien, C., Delaux, P., Strother, P. K., Kenrick, P., Selosse, M., & Taylor, J. W. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0426-8 · Cited by 106 · see citing works
Pervasive aerobic nitrogen cycling in the surface ocean across the Paleoproterozoic Era
Kipp, M. A., Stüeken, E. E., Yun, M., Bekker, A., & Buick, R. (2018) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2018.08.007 · Cited by 104 · see citing works
Ediacaran reorganization of the marine phosphorus cycle
Laakso, T. A., Sperling, E. A., Johnston, D. T., & Knoll, A. H. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1916738117 · Cited by 100 · see citing works
Tracking the rise of eukaryotes to ecological dominance with zinc isotopes
Isson, T. T., Love, G. D., Dupont, C. L., Reinhard, C. T., Zumberge, A. J., Asael, D., Gueguen, B., McCrow, J., Gill, B. C., Owens, J., et al. (2018) · Geobiology · doi:10.1111/gbi.12289 · Cited by 101 · see citing works
Jackson, C., Knoll, A. H., Chan, C. X., & Verbruggen, H. (2018) · Scientific Reports · doi:10.1038/s41598-017-18805-w · Cited by 99 · see citing works
Cavalier-Smith, T., Chao, E., & Lewis, R. (2018) · Protoplasma · doi:10.1007/s00709-018-1241-1 · Cited by 79 · see citing works
The origin and early evolution of plants
Bowles, A. M. C., Williamson, C. J., Williams, T. A., Lenton, T. M., & Donoghue, P. C. J. (2022) · Trends in Plant Science · doi:10.1016/j.tplants.2022.09.009 · Cited by 93 · see citing works
Heterogeneous and dynamic marine shelf oxygenation and coupled early animal evolution
Li, C., Cheng, M., Zhu, M., & Lyons, T. W. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170157 · Cited by 98 · see citing works
Carbonates before skeletons: A database approach
Cantine, M. D., Knoll, A. H., & Bergmann, K. (2019) · Earth-Science Reviews · doi:10.1016/j.earscirev.2019.103065 · Cited by 97 · see citing works
Diachronous development of Great Unconformities before Neoproterozoic Snowball Earth
Flowers, R. M., Macdonald, F. A., Siddoway, C. S., & Havranek, R. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913131117 · Cited by 99 · see citing works
Primary Productivity Was Limited by Electron Donors Prior to the Advent of Oxygenic Photosynthesis
Ward, L. M., Rasmussen, B., & Fischer, W. W. (2018) · Journal of Geophysical Research Biogeosciences · doi:10.1029/2018jg004679 · Cited by 91 · see citing works
Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals
Nettersheim, B. J., Brocks, J. J., Schwelm, A., Hope, J. M., Not, F., Lomas, M. W., Schmidt, C., Schiebel, R., Nowack, E. C. M., Patrick De Deckker, B., et al. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0806-5 · Cited by 91 · see citing works
Self-citationParsons, C., Stüeken, E. E., Rosen, C. J., Mateos, K., & Anderson, R. E. (2021) · Geobiology · doi:10.1111/gbi.12419 · Cited by 91 · see citing works
Bykova, N., LoDuca, S. T., Ye, Q., Marusin, V. V., Grazhdankin, D. V., & Xiao, S. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.105875 · Cited by 90 · see citing works
Oxygen, animals and aquatic bioturbation: An updated account
Butterfield, N. J. (2018) · Geobiology · doi:10.1111/gbi.12267 · Cited by 89 · see citing works
Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)
Sánchez‐Baracaldo, P., Bianchini, G., Cesare, A. D., Callieri, C., & Chrismas, N. A. M. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00045 · Cited by 81 · see citing works
Hydrological controls on marine chemistry in the Cryogenian Nanhua Basin (South China)
Cheng, M., Zhang, Z., Algeo, T. J., Liu, S., Liu, X., Wang, H., Chang, B., Jin, C., Pan, W., Cao, M., et al. (2021) · Earth-Science Reviews · doi:10.1016/j.earscirev.2021.103678 · Cited by 90 · see citing works
Evolution of bacterial steroid biosynthesis and its impact on eukaryogenesis
Hoshino, Y., & Gaucher, E. A. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101276118 · Cited by 83 · see citing works
Self-citationWei, G., Wei, W., Wang, D., Li, T., Yang, X., Shields, G., Zhang, F., Li, G., Chen, T., Yang, T., et al. (2020) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2020.116244 · Cited by 86 · see citing works
Evolution of the structure and impact of Earth’s biosphere
Planavsky, N. J., Crowe, S. A., Fakhraee, M., Beaty, B., Reinhard, C. T., Mills, B. J. W., Holstege, C., & Konhauser, K. O. (2021) · Nature Reviews Earth & Environment · doi:10.1038/s43017-020-00116-w · Cited by 100 · see citing works
Evolution of the Cholesterol Biosynthesis Pathway in Animals
Zhang, T., Yuan, D., Xie, J., Lei, Y., Li, J., Fang, G., Tian, L., Liu, J., Cui, Y., Zhang, M., et al. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz167 · Cited by 85 · see citing works
Evidence for high organic carbon export to the early Cambrian seafloor
Cheng, M., Li, C., Jin, C., Wang, H., Algeo, T. J., Lyons, T. W., Zhang, F., & Anbar, A. D. (2020) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2020.01.050 · Cited by 84 · see citing works
Xia, L., Cao, J., Hu, W., Zhi, D., Tang, Y., Li, E., & He, W. (2020) · Earth-Science Reviews · doi:10.1016/j.earscirev.2020.103499 · Cited by 86 · see citing works
What the ~1.4 Ga Xiamaling Formation can and cannot tell us about the mid‐Proterozoic ocean
Diamond, C., Planavsky, N. J., Wang, C., & Lyons, T. W. (2018) · Geobiology · doi:10.1111/gbi.12282 · Cited by 84 · see citing works
Nitrogen isotope constraints on the early Ediacaran ocean redox structure
Wang, X., Jiang, G., Shi, X., Peng, Y., & Morales, D. C. (2018) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2018.08.034 · Cited by 83 · see citing works
The geologic history of primary productivity
Crockford, P. W., On, Y. M. B., Ward, L. M., Milo, R., & Halevy, I. (2023) · Current Biology · doi:10.1016/j.cub.2023.09.040 · Cited by 76 · see citing works
Cheng, M., Li, C., Chen, X., Zhou, L., Algeo, T. J., Ling, H.-F., Feng, L.-J., & Jin, C.-S. (2018) · Precambrian Research · doi:10.1016/j.precamres.2017.12.007 · Cited by 77 · see citing works
Hoffman, P. F., Halverson, G. P., Schrag, D. P., Higgins, J. A., Domack, E. W., Macdonald, F. A., Pruss, S. B., Blättler, C. L., Crockford, P. W., Hodgin, E. B., et al. (2021) · Earth-Science Reviews · doi:10.1016/j.earscirev.2021.103616 · Cited by 78 · see citing works
The origin of phagocytosis in Earth history
Mills, D. B. (2020) · Interface Focus · doi:10.1098/rsfs.2020.0019 · Cited by 78 · see citing works
Ward, L. M., & Shih, P. M. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.049 · Cited by 74 · see citing works
Pehr, K., Love, G. D., Кузнецов, А. Б., Podkovyrov, V. N., Junium, C. K., Shumlyanskyy, L. V., Sokur, T. M., & Bekker, A. (2018) · Nature Communications · doi:10.1038/s41467-018-04195-8 · Cited by 75 · see citing works
Luo, G., Junium, C. K., Izon, G., Ono, S., Beukes, N. J., Algeo, T. J., Cui, Y., Xie, S., & Summons, R. E. (2018) · Nature Communications · doi:10.1038/s41467-018-03361-2 · Cited by 75 · see citing works
Organic carbon cycling and black shale deposition: an Earth System Science perspective
Jin, Z., Wang, X., Wang, H., Ye, Y., & Zhang, S. (2023) · National Science Review · doi:10.1093/nsr/nwad243 · Cited by 75 · see citing works
The transition from a cyanobacterial to algal world and the emergence of animals
Brocks, J. J. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20180039 · Cited by 74 · see citing works
Self-citationHoffman, P. F., & Lamothe, K. G. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1909570116 · Cited by 74 · see citing works
Zumberge, J. A., Rocher, D., & Love, G. D. (2020) · Geobiology · doi:10.1111/gbi.12378 · Cited by 73 · see citing works
Neoproterozoic geochronology and provenance of the Adelaide Superbasin
Lloyd, J., Blades, M., Counts, J. W., Collins, A. S., Amos, K. J., Wade, B. P., Hall, J. W., Hore, S., Ball, A. M., Shahin, S., et al. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.105849 · Cited by 75 · see citing works
A crown-group cnidarian from the Ediacaran of Charnwood Forest, UK
Dunn, F. S., Kenchington, C. G., Parry, L. A., Clark, J., Kendall, R. S., & Wilby, P. R. (2022) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01807-x · Cited by 75 · see citing works
A small marine biosphere in the Proterozoic
Laakso, T. A., & Schrag, D. P. (2018) · Geobiology · doi:10.1111/gbi.12323 · Cited by 71 · see citing works
The impact of marine nutrient abundance on early eukaryotic ecosystems
Reinhard, C. T., Planavsky, N. J., Ward, B. A., Love, G. D., Hir, G. L., & Ridgwell, A. J. (2020) · Geobiology · doi:10.1111/gbi.12384 · Cited by 73 · see citing works
Chen, Y., Diamond, C., Stüeken, E. E., Cai, C., Gill, B. C., Zhang, F., Bates, S. M., Chu, X., Ding, Y., & Lyons, T. W. (2019) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2019.05.017 · Cited by 68 · see citing works
The Evolution Pathway of Ammonia-Oxidizing Archaea Shaped by Major Geological Events
Yang, Y., Zhang, C., Lenton, T. M., Yan, X., Zhu, M., Zhou, M., Tao, J., Phelps, T. J., & Cao, Z. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab129 · Cited by 64 · see citing works
Cavalier‐Smith, T., & Chao, E. E. Y. (2020) · PROTOPLASMA · doi:10.1007/s00709-019-01442-7 · Cited by 68 · see citing works
The history of Earth’s sulfur cycle
Fakhraee, M., Crockford, P. W., Bauer, K. W., Pasquier, V., Sugiyama, I., Katsev, S., Raven, M. R., Gomes, M. L., Philippot, P., Crowe, S. A., et al. (2024) · Nature Reviews Earth & Environment · doi:10.1038/s43017-024-00615-0 · Cited by 69 · see citing works
Xiao, S., & Tang, Q. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170165 · Cited by 64 · see citing works
Palaeoproterozoic oxygenated oceans following the Lomagundi–Jatuli Event
Mänd, K., Lalonde, S. V., Robbins, L. J., Thoby, M., Paiste, K., Kreitsmann, T., Paiste, P., Reinhard, C. T., Romashkin, A. E., Planavsky, N. J., et al. (2020) · Nature Geoscience · doi:10.1038/s41561-020-0558-5 · Cited by 68 · see citing works
Xiao, D., Cao, J., Luo, B., Tan, X., Xiao, W., He, Y., & Li, K. (2020) · Earth-Science Reviews · doi:10.1016/j.earscirev.2020.103453 · Cited by 65 · see citing works
Collins, A. S., Blades, M. L., Merdith, A., & Foden, J. (2021) · Communications Earth & Environment · doi:10.1038/s43247-021-00149-z · Cited by 66 · see citing works
Marine biogeochemical nitrogen cycling through Earth’s history
Stüeken, E. E., Pellerin, A., Thomazo, C., Johnson, B., Duncanson, S. P., & Schoepfer, S. D. (2024) · Nature Reviews Earth & Environment · doi:10.1038/s43017-024-00591-5 · Cited by 67 · see citing works
COHEN, P. A., & Kodner, R. B. (2021) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2021.11.005 · Cited by 65 · see citing works
C-4 sterol demethylation enzymes distinguish bacterial and eukaryotic sterol synthesis
Lee, A. K., Banta, A. B., Wei, J. H., Kiemle, D. J., Feng, J., Giner, J., & Welander, P. V. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802930115 · Cited by 63 · see citing works
Paleoenvironmental proxies and what the Xiamaling Formation tells us about the mid‐Proterozoic ocean
Zhang, S., Wang, X., Wang, H., Bjerrum, C. J., Hammarlund, E. U., Haxen, E. R., Wen, H., Ye, Y., & Canfield, D. E. (2019) · Geobiology · doi:10.1111/gbi.12337 · Cited by 62 · see citing works
Zhao, W., Wang, X., Hu, S., Zhang, S., Wang, H., Guan, S., Ye, Y., Ren, R., & Wang, T. (2019) · Science China Earth Sciences · doi:10.1007/s11430-018-9312-4 · Cited by 63 · see citing works
Implications for Ediacaran biological evolution from the ca. 602 Ma Lantian biota in China
Yang, C., Li, Y., Selby, D. S., Wan, B., Guan, C., Zhou, C., & Li, X. (2022) · Geology · doi:10.1130/g49734.1 · Cited by 61 · see citing works
Loron, C., Rainbird, R. H., Turner, E. C., Greenman, J. W., & Javaux, E. (2018) · Precambrian Research · doi:10.1016/j.precamres.2018.12.024 · Cited by 59 · see citing works
Cryogenian cap carbonate models: a review and critical assessment
Yu, W., Algeo, T. J., Zhou, Q. F., Du, Y., & Wang, P. (2020) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2020.109727 · Cited by 58 · see citing works
The Mesoproterozoic Oxygenation Event
Zhang, S., Wang, H., Wang, X., & Ye, Y. (2021) · Science China Earth Sciences · doi:10.1007/s11430-020-9825-x · Cited by 60 · see citing works
Lenton, T. M., & Daines, S. J. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170156 · Cited by 55 · see citing works
Subglacial meltwater supported aerobic marine habitats during Snowball Earth
Lechte, M. A., Wallace, M. W., Hood, A. V. S., Li, W., Jiang, G., Halverson, G. P., Asael, D., McColl, S. L., & Planavsky, N. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1909165116 · Cited by 56 · see citing works
Niche expansion for phototrophic sulfur bacteria at the Proterozoic–Phanerozoic transition
Cui, X., Liu, X., Shen, G., Ma, J., Husain, F., Rocher, D., Zumberge, J. E., Bryant, D. A., & Summons, R. E. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006379117 · Cited by 56 · see citing works
Algal origin of sponge sterane biomarkers negates the oldest evidence for animals in the rock record
Bobrovskiy, I., Hope, J. M., Nettersheim, B. J., Volkman, J. K., Hallmann, C., & Brocks, J. J. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-01334-7 · Cited by 57 · see citing works
Self-citationLaakso, T. A., & Schrag, D. P. (2018) · Global Biogeochemical Cycles · doi:10.1002/2017gb005832 · Cited by 55 · see citing works
Ma, Z., Liu, X., Yu, W., Du, Y., & Du, Q. (2019) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2019.05.031 · Cited by 55 · see citing works
A largely invariant marine dissolved organic carbon reservoir across Earth's history
Fakhraee, M., Tarhan, L. G., Planavsky, N. J., & Reinhard, C. T. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2103511118 · Cited by 55 · see citing works
1.63-billion-year-old multicellular eukaryotes from the Chuanlinggou Formation in North China
Miao, L., Yin, Z., Knoll, A. H., Qu, Y., & Zhu, M. (2024) · Science Advances · doi:10.1126/sciadv.adk3208 · Cited by 55 · see citing works
Nguyen, K. D., Love, G. D., Zumberge, J. A., Kelly, A. E., Owens, J. D., Rohrssen, M., Bates, S. M., Cai, C., & Lyons, T. W. (2019) · Geobiology · doi:10.1111/gbi.12329 · Cited by 55 · see citing works
Petrographic carbon in ancient sediments constrains Proterozoic Era atmospheric oxygen levels
Canfield, D., van Zuilen, M. V., Nabhan, S., Bjerrum, C., Zhang, S.-C., Wang, H.-J., & Wang, X.-M. (2021) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2101544118 · Cited by 45 · see citing works
Wei, G., Zhao, M., Sperling, E. A., Gaines, R. R., Kalderon-Asael, B., Shen, J., Li, C., Zhang, F., Li, G., Zhou, C., et al. (2024) · Science Advances · doi:10.1126/sciadv.adk2152 · Cited by 54 · see citing works
Hou, Z., Ma, X., Shi, X., Li, X., Yang, L., Xiao, S., Clerck, O. D., Leliaert, F., & Zhong, B. (2022) · Nature Communications · doi:10.1038/s41467-022-29282-9 · Cited by 52 · see citing works
Zhu, Z., Campbell, I. H., Allen, C. M., Brocks, J. J., & Chen, B. (2022) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2022.117391 · Cited by 52 · see citing works
Self-citationVinnichenko, G., Jarrett, A. J. M., Hope, J. M., & Brocks, J. J. (2020) · Geobiology · doi:10.1111/gbi.12390 · Cited by 51 · see citing works
Self-citationHoltvoeth, J., Whiteside, J. H., Engels, S., de Freitas, F. S., Grice, K., Greenwood, P. F., Johnson, S., Kendall, I. P., Lengger, S. K., Lücke, A., et al. (2019) · Quaternary Science Reviews · doi:10.1016/j.quascirev.2019.01.001 · Cited by 51 · see citing works
Mid-Proterozoic redox evolution and the possibility of transient oxygenation events
Diamond, C. W., & Lyons, T. W. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170146 · Cited by 49 · see citing works
- Authors
- Brocks, J. J., Jarrett, A. J. M., Sirantoine, E., Hallmann, C., Hoshino, Y., & Liyanage, T.
- Affiliations
- Australian National University (AU)
- University of Bremen (DE)
- Max Planck Institute for Biogeochemistry (DE)
- Corresponding author
- Brocks, Jochen J.
- ORCID
- Venue
- Nature
- Published
- 2017-08
- Volume
- 548
- Issue
- 7669
- Pages
- 578-581
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2749763761
- Cited by
- 574
- References
- 42
- Citations by year
- 2026: 48 · 2025: 59 · 2024: 57 · 2023: 66 · 2022: 68 · 2021: 80 · 2020: 69 · 2019: 62 · 2018: 54 · 2017: 11
- FWCI
- 38.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Publication Database GFZ (GFZ German Research Centre for Geosciences) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Australian National University
- Australian Research Council
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- Cryogenian, Ediacaran, molecular fossils, Archaeplastida, phytoplankton, Snowball Earth, Sturtian glaciation, Marinoan glaciation, cyanobacteria, atmospheric oxygen, food webs, origin of animals
- MeSH terms
- Cyanobacteria, Animals, Fossils, Oceans and Seas, Phosphorus, Biomarkers, Food Chain, Ice Cover, History, Ancient, Eukaryota, Carbon Cycle
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
