Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China
Open accessAbstract
Fossils of macroscopic eukaryotes are rarely older than the Ediacaran Period (635–541 million years (Myr)), and their interpretation remains controversial. Here, we report the discovery of macroscopic fossils from the 1,560-Myr-old Gaoyuzhuang Formation, Yanshan area, North China, that exhibit both large size and regular morphology. Preserved as carbonaceous compressions, the Gaoyuzhuang fossils have statistically regular linear to lanceolate shapes up to 30 cm long and nearly 8 cm wide, suggesting that the Gaoyuzhuang fossils record benthic multicellular eukaryotes of unprecedentedly large size. Syngenetic fragments showing closely packed ∼10 μm cells arranged in a thick sheet further reinforce the interpretation. Comparisons with living thalloid organisms suggest that these organisms were photosynthetic, although their phylogenetic placement within the Eukarya remains uncertain. The new fossils provide the strongest evidence yet that multicellular eukaryotes with decimetric dimensions and a regular developmental program populated the marine biosphere at least a billion years before the Cambrian Explosion.
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Eukaryotic multicellularity at ~1.6 Ga followed soon after the 1.7 to 1.6 Ga stem eukaryote remains.
“Eukaryotic multicellularity at ∼1.6 Ga followed soon after those 1.7 to 1.6 Ga stem eukaryote remains (Zhu et al., 2016)”
From Oxygenation, Life, and the Planetary System during Earth's Middle History: An Overview (2021) · cites this paper as Zhu et al., 2016
The Discussion (page unavailable) concludes that eukaryotes had evolved multicellularity by about 1.6 Ga. The paper also mentions older North China fossils, but says their cellular structure and affinities are uncertain; it does not establish them as 1.7–1.6 Ga stem-eukaryote remains or explicitly link the Gaoyuzhuang fossils to them. (LLM, conf=0.86)
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Zhang, H., LinZhi, G., HongRui, Z., Biao, S., XiaoZhong, D., Chuan-heng, Z., HaoGang, L., & ChengQiang, G. (2019) · Acta Petrologica Sinica · doi:10.18654/1000-0569/2019.08.10 · Cited by 31 · see citing works
Wang, Z., Wang, X., Shi, X., Tang, D., Stüeken, E. E., & Song, H. (2020) · Journal of Geophysical Research Biogeosciences · doi:10.1029/2019jg005487 · Cited by 31 · see citing works
“Indeed, in the middle part of Member III where most eukaryotic fossils were discovered (Shi et al., 2017; Zhu et al., 2016), the enrichments of some RSEs (e.g., Mo, V, and U) show an apparent increase from low background values (Figure 5), possibly indicative of an increased RSEs pool in seawater…”
BackgroundInfluentialMesoproterozoic marine biological carbon pump: Source, degradation, and enrichment of organic matter
Zhang, S., Wang, H., Wang, X., & Ye, Y. (2022) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/tb-2022-0041 · Cited by 30 · see citing works
Frameworks for Interpreting the Early Fossil Record of Eukaryotes
Porter, S. M., & Riedman, L. A. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032421-113254 · Cited by 29 · see citing works
A case for an active eukaryotic marine biosphere during the Proterozoic era
Eckford-Soper, L., Andersen, K. H., Hansen, T. F., & Canfield, D. E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122042119 · Cited by 28 · see citing works
“Q. Luo, S. C. George, Y. Xu, N. Zhong, Organic geochemical characteristics of the Mesoproterozoic Hongshuizhuang Formation from northern China: Implications for thermal maturity and biological sources.”
BackgroundInfluentialEmergence of Hierarchical Modularity in Evolving Networks Uncovered by Phylogenomic Analysis
Caetano‐Anollés, G., Aziz, M. F., Mughal, F., Gräter, F., Koç, İ., Caetano-Anollés, K., & Caetano-Anollés, D. (2019) · Evolutionary Bioinformatics · doi:10.1177/1176934319872980 · Cited by 27 · 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 Proterozoic macrofossil Tawuia as a coenocytic eukaryote and a possible macroalga
Tang, Q., Pang, K., Li, G., Chen, L., Yuan, X., Шарма, М., & Xiao, S. (2021) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2021.110485 · Cited by 27 · see citing works
Hu, J., Li, C., Tong, J., Ye, Q., Tian, L., An, Z., Dodd, M. S., & Algeo, T. J. (2020) · Precambrian Research · doi:10.1016/j.precamres.2020.105969 · Cited by 26 · see citing works
Zhang, S., Cao, R., Lan, Z., Li, Z., Zhao, Z., Wan, B., Guan, C., & Yuan, X. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106562 · Cited by 26 · see citing works
Lyu, D., Deng, Y., Wang, X., Ye, Y., Pang, K., Miao, L., Luo, Z., Zhang, F., Lu, Y., Deng, S., et al. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106577 · Cited by 26 · see citing works
WenLin, G., Su, W., Zhang, J., Li, H., HongYing, Z., Li, H., Ettensohn, F. R., & Huff, W. D. (2019) · Acta Petrologica Sinica · doi:10.18654/1000-0569/2019.08.08 · Cited by 25 · see citing works
Four series of rearranged hopanes in the Mesoproterozoic sediments
Xiao, H., Li, M., Wang, T., You, B., Leng, J., Han, Q., Ran, Z., Wang, X., & Gao, Z. (2021) · Chemical Geology · doi:10.1016/j.chemgeo.2021.120210 · Cited by 24 · see citing works
“7a) (Yan and Liu, 1998), decimeter-scale multicellular macroscopic eukaryotes (Zhu et al., 2016), and striking steranes biomarkers (Li et al., 2003) were discovered in the sediments of Gaoyuzhuang Formation (1.56 Ga), but which only contain trace amounts of rearranged hopanes, even below the…”
InfluentialShi, 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
The Paleo-Mesoproterozoic boundary: 1.8Ga
TaiPing, Z., LanYin, P., YiFan, Q., XiYan, Z., ShiYan, W., & YuanSheng, G. (2019) · Acta Petrologica Sinica · doi:10.18654/1000-0569/2019.08.01 · Cited by 22 · see citing works
Agić, H., Högström, A. E. S., Moczydłowska, M., Jensen, S., Palacios, T., Meinhold, G., Ebbestad, J. O. R., Taylor, W. L., & Høyberget, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-50650-x · Cited by 21 · see citing works
Li, D., Luo, G., Tang, Q., She, Z., & Xiao, S. (2023) · Precambrian Research · doi:10.1016/j.precamres.2023.107104 · Cited by 20 · see citing works
Ding, T., Gao, J., Tian, S., Fan, C., Zhao, Y., Wan, D. F., & Zhou, J. (2017) · Scientific Reports · doi:10.1038/srep44000 · Cited by 21 · see citing works
Nutrient-dependent growth underpinned the Ediacaran transition to large body size
Cuthill, J. F. H., & Morris, S. C. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0222-7 · Cited by 20 · see citing works
Yang, B., Collins, A. S., Blades, M., Munson, T. J., Payne, J. L., Glorie, S., & Farkaš, J. (2020) · Geological Magazine · doi:10.1017/s0016756820001223 · Cited by 18 · see citing works
Was There a Cambrian Explosion on Land? The Case of Arthropod Terrestrialization
Tihelka, E., Howard, R. J., Cai, C., & Lozano-Fernández, J. (2022) · Biology · doi:10.3390/biology11101516 · Cited by 18 · see citing works
“However, the emergence of complex multicellular organisms, such as animals, plants and fungi, only occurred during the last 1000 million years [5] (but see [6] for older estimates).”
BackgroundA review of microbial‐environmental interactions recorded in Proterozoic carbonate‐hosted chert
Moore, K. R., Daye, M., Gong, J., Williford, K. H., Konhauser, K. O., & Bosak, T. (2022) · Geobiology · doi:10.1111/gbi.12527 · Cited by 18 · see citing works
Ossa, F. O., Pons, M., Bekker, A., Hofmann, A., Poulton, S. W., Andersen, M. B., Agangi, A., Gregory, D. D., Reinke, C., Steinhilber, B., et al. (2023) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2023.118147 · Cited by 18 · see citing works
Systematic paleontology of macroalgal fossils from the Tonian Mackenzie Mountains Supergroup
Maloney, K. M., Maverick, D. P., Schiffbauer, J. D., Halverson, G. P., Xiao, S., & Laflamme, M. (2023) · Journal of Paleontology · doi:10.1017/jpa.2023.4 · Cited by 17 · see citing works
“The ca. 1560 Ma Gaoyuzhuang biota of North China includes large carbonaceous compressions that have also been interpreted as algae (Zhu et al., 2016), but in the absence of cellular preservation or other morphologically informative characters, their phylogenetic placement within broader algae…”
BackgroundOrganic geochemical compositions of Mesoproterozoic source rocks in the Yanliao Rift, Northern China
Song, D., Chen, Y., Wang, T., Li, M., & Li, P. (2020) · Marine and Petroleum Geology · doi:10.1016/j.marpetgeo.2020.104740 · Cited by 17 · see citing works
Ediacaran macrofossils prior to the ~580 Ma Gaskiers glaciation in Newfoundland, Canada
Liu, A., & Tindal, B. H. (2020) · Lethaia · doi:10.1111/let.12401 · Cited by 16 · see citing works
“problematic taxa (Fedonkin & Yochelson 2002) or comprise simple algal‐like (Ye et al. 2015; Zhu et al. 2016) or discoidal impressions (e.”
BackgroundTao, J., Zhang, J., Liu, Y., Stüeken, E. E., Dong, Z., Shi, M., Li, P., Zhang, Q., & Poulton, S. W. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106868 · Cited by 16 · see citing works
Self-citationA rare disc-like holdfast of the Ediacaran macroalga from South China
Wang, Y., Wang, Y., & Du, W. (2017) · Journal of Paleontology · doi:10.1017/jpa.2017.43 · Cited by 16 · see citing works
“7.6) were reported by Zhu et al. (2016), but no detailed description of the two specimens was provided.”
BackgroundInfluentialTemporal and spatial distribution of Precambrian red beds and their formation mechanisms
Kuang, H., Bai, H., Peng, N., Qi, K., Wang, Y., Chen, X., & Liu, Y. (2022) · Geosystems and Geoenvironment · doi:10.1016/j.geogeo.2022.100098 · Cited by 15 · 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
Ediacaran macroalgal holdfasts and their evolution: a case study from China
Wang, Y., Tang, F., Tang, F., & Zhao, M. (2020) · Palaeontology · doi:10.1111/pala.12485 · Cited by 14 · see citing works
“7E; see Zhu et al. 2016, fig.”
BackgroundInfluentialJia, T., Wang, R., Huang, T., Lang, X., Ma, H., & Shen, B. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106681 · Cited by 14 · see citing works
Fluctuating oxygenation and dynamic iron cycling in the late Paleoproterozoic ocean
Yang, X., Mao, J., Li, R., Huang, F., He, C., Zhao, C., Wei, W., Yang, G., Xiong, Y., & Poulton, S. W. (2023) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2023.118554 · Cited by 16 · see citing works
Liu, J., Zhang, Y., Shi, X., Chen, A., Tang, D., & Yang, T. (2023) · Palaeontology · doi:10.1111/pala.12685 · Cited by 12 · see citing works
Choudhuri, A., Banerjee, S., & SARKAR, S. (2020) · Journal of Mineralogical and Petrological Sciences · doi:10.2465/jmps.190827a · Cited by 13 · see citing works
“…cf. Franceville biota of 2.1 Ga (El Albani et al., 2010, 2014), Stirling biota of ~ 1.8 Ga (Bengtson et al., 2017), Montana biota of 1.5–1.3 Ga (Zhu et al., 2016), and motile organisms from 2.1 Ga old rocks (El Albani et al., 2019), inspire a re–assessment of the Vindhyan metazoan records for…”
BackgroundInfluentialLiu, G., Zhang, S., Li, H., Bao, X., Zhao, H., Liang, D., Wu, H., Tang, D., Zhu, X., & Yang, T. (2022) · Global and Planetary Change · doi:10.1016/j.gloplacha.2022.103916 · Cited by 13 · see citing works
Jing, Y., Chen, Z., Anderson, R. P., Wang, X., Zemin, Z., & Feng, X. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106899 · Cited by 13 · see citing works
Li, G., Chen, L., Pang, K., Tang, Q., Wu, C., Yuan, X., Zhou, C., & Xiao, S. (2023) · Communications Biology · doi:10.1038/s42003-023-04740-2 · Cited by 13 · see citing works
“…examples of early Mesoproterozoic or earlier mac-rofossils include the helical fossils Grypania and Katnia 75,76 , the tomaculate fossil Tawuia 75 , and unnamed carbonaceous fossils from the 1.56 Ga Gaoyuzhuang Formation of North China 77 , all of which have been known as carbonaceous compressions.”
InfluentialMegascopic Carbonaceous Remains from Proterozoic Basins of India
Шарма, М., & Singh, V. K. (2018) · Society of Earth Scientists series · doi:10.1007/978-3-319-89698-4_27 · Cited by 12 · see citing works
Zhang, F., Wang, H., Ye, Y., Deng, Y., Lyu, Y., Wang, X., Yu, Z., Lyu, D., Lu, Y., Zhou, C., et al. (2021) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2021.110449 · Cited by 12 · see citing works
Wang, X., Zhang, S., Ye, Y., Ma, S., Su, J., Wang, H., & Canfield, D. E. (2023) · Earth-Science Reviews · doi:10.1016/j.earscirev.2023.104499 · Cited by 12 · see citing works
Description of MethodsPreprint
Sauseng, P. (2015) · doi:10.17605/osf.io/v5bu7 · Cited by 12 · see citing works
Large igneous provinces played a major role in oceanic oxygenation events during the mid-Proterozoic
Luo, A., Sun, G., Grasby, S. E., & Yin, R. (2024) · Communications Earth & Environment · doi:10.1038/s43247-024-01780-2 · Cited by 11 · see citing works
“However, growing evidence supports that the redoxstateofthemid-Proterozoicwaslikelydynamic,withseveralintervals ofhighoxygenlevelsthatpunctuatedoveralllowbackgroundlevels 2 – 10 .”
Mo-Ni and organic carbon isotope signatures of the mid-late Mesoproterozoic oxygenation
Ansari, A. H., Ahmad, S., Govil, P., Agrawal, S., & Mathews, R. P. (2019) · Journal of Asian Earth Sciences · doi:10.1016/j.jseaes.2019.104201 · Cited by 11 · see citing works
Did high temperature rather than low O2 hinder the evolution of eukaryotes in the Precambrian?
Zhang, F., Wang, H., Ye, Y., Liu, Y., Lyu, Y., Deng, Y., Lyu, D., Wang, X., Wu, H., Deng, S., et al. (2022) · Precambrian Research · doi:10.1016/j.precamres.2022.106755 · Cited by 11 · see citing works
Proterozoic microfossils continue to provide new insights into the rise of complex eukaryotic life
Anderson, R. P., Mughal, S., & Wedlake, G. O. (2024) · Royal Society Open Science · doi:10.1098/rsos.240154 · Cited by 9 · see citing works
“…Ma [99–101], carbonaceous forms such as Grypania ~1900 Ma [102] and Katnia ~1600 Ma [103] and decimetre-scale blade-like carbonaceous compressions [104,105] have also all been allied to eukaryotes but without conclusive evidence; other origins either as bacteria or as non-biogenic structures…”
BackgroundIsotopic evidence for oceanic barium cycling in the initial stage of the mesoproterozoic
Li, X., Crockford, P. W., Song, Y., Yin, H., Wei, W., Wang, X., Ye, Y., Jing, Z., Huang, F., Wang, H., et al. (2025) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2025.119314 · Cited by 11 · see citing works
Great Canadian Lagerstätten 6. Mistaken Point Ecological Reserve, Southeast Newfoundland
Liu, A., & Matthews, J. J. (2017) · Geoscience Canada · doi:10.12789/geocanj.2017.44.117 · Cited by 8 · see citing works
“…while evidence for testate amoebae (Bosak et al. 2011a), ciliates (Bosak et al. 2011b), foraminifera (Bosak et al. 2012), and largely sub-centimetric algae (Butterfield 2009; Zhu et al. 2016), fungi (Butterfield 2005) and rare putative animals (Yin et al. 2015) all predates the Ediacaran period.”
BackgroundWang, X., Jing, Y., Peng, H., Yang, H., Zhu, Z., & Chen, Z. (2023) · Precambrian Research · doi:10.1016/j.precamres.2023.107021 · Cited by 10 · see citing works
Zhang, J., Li, H., Tian, H., Liu, H., HongYing, Z., & WenGang, L. (2021) · Acta Petrologica Sinica · doi:10.18654/1000-0569/2021.01.14 · Cited by 10 · see citing works
Self-citationExtended series of tricyclic terpanes in the Mesoproterozoic sediments
Xiao, H. B., Wang, T., Li, M., You, B., & Zhu, Z. (2021) · Organic Geochemistry · doi:10.1016/j.orggeochem.2021.104245 · Cited by 10 · see citing works
Ye, Y., Wang, H., Wang, X., Li, J., Wu, C., & Zhang, S. (2022) · Geosystems and Geoenvironment · doi:10.1016/j.geogeo.2022.100173 · Cited by 10 · see citing works
- Authors
- Zhu, S., Zhu, M., Knoll, A. H., Yin, Z., Zhao, F., Sun, S., Qu, Y., Shi, M., & Liu, H.
- Affiliations
- China Geological Survey (CN)
- Chinese Academy of Sciences (CN)
- Harvard University (US)
- University of Bergen (NO)
- China University of Geosciences (CN)
- Corresponding author
- Zhu, Maoyan
- Venue
- Nature Communications
- Published
- 2016-05-17
- Volume
- 7
- Issue
- 1
- Pages
- 11500-11500
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC4873660
- OpenAlex
- W2396542812
- Cited by
- 199
- References
- 37
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 25 · 2023: 19 · 2022: 30 · 2021: 25 · 2020: 17 · 2019: 14 · 2018: 13 · 2017: 17 · 2016: 4 · 2015: 1
- FWCI
- 13.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Aeronautics and Space Administration
- National Natural Science Foundation of China (41272015)
- NASA Astrobiology Institute
- China Geological Survey
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- multicellular eukaryotes, Ediacaran fossils, Gaoyuzhuang Formation, photosynthetic organisms, Cambrian explosion, early eukaryotic evolution
- MeSH terms
- China, Fossils, Spectrum Analysis, Raman, Time Factors, Geologic Sediments, Eukaryota
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