Skip to main content
SpringerLink
Log in

Ultrastructure and in-situ chemical characterization of intracellular granules of embryo-like fossils from the early Ediacaran Weng’an biota

  • Research Paper
  • Published:
PalZ Aims and scope Submit manuscript

Abstract

Embryo-like fossils from the early Ediacaran Weng’an biota provide a window of exceptional fossil preservation onto the period of life history in which molecular clocks estimate the fundamental animal lineages to have diverged. However, their diversity and biological affinities have proven controversial, because they are morphologically simple and, consequently, their interpretation lacks phylogenetic constraint. The subcellular structures preserved in these embryo-like fossils might help to understand their cytology, biology, and diversity, but the potential of these structures has not been fully realized, because detailed microscale physical and chemical investigations are lacking. Here, to remedy this deficiency, we performed a comprehensive study to characterize their micro- and ultra-structures as well as in-situ chemical components. Our results reveal three types of subcellular structure that differ in size, shape, and mineral components: (1) relatively small and spheroidal granules in embryo-like fossils with equal cell division pattern; (2) relatively large, spheroidal, or polygonal granules in embryo-like fossils with unequal and asynchronous cell division pattern; and (3) irregular multi-layered rim-bounded granules in embryo-like fossils with unequal and asynchronous cell division pattern. We propose that the three types may be rationalized to a single taphonomic pathway of preferential mineralization of the cell cytoplasm, preserving an external mould of subcellular granules. We followed the previous interpretation that the spheroidal and polygonal granules should be fossilized lipid droplets or yolk platelets. The distinction between these subcellular structures are largely the result of postmortem degradation processes such as autolysis. The widely preserved lipid droplets or yolk platelets within these Ediacaran embryo-like fossils are compatible with the interpretion of large yolky embryos with maternal nourishment and direct development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bailey, J.V., S.B. Joye, K.M. Kalanetra, B.E. Flood, and F.A. Corsetti. 2007. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites. Nature 445: 198–201.

    Article  Google Scholar 

  • Bailleul, A.M. 2021. Fossilized cell nuclei are not that rare: review of the histological evidence in the Phanerozoic. Earth-Science Reviews 216: 103599.

    Article  Google Scholar 

  • Bottjer, D.J., Z.J. Yin, F.C. Zhao, and M.Y. Zhu. 2020. Comparative taphonomy and phylogenetic signal of phosphatized Weng’an and Kuanchuanpu Biotas. Precambrian Research 349: 105408.

    Article  Google Scholar 

  • Carlisle, E.M., M. Jobbins, V. Pankhania, J.A. Cunningham, and P.C.J. Donoghue. 2021. Experimental taphonomy of organelles and the fossil record of early eukaryote evolution. Science Advances 7: eabe9487.

    Article  Google Scholar 

  • Chen, J.Y., P. Oliveri, C.W. Li, G.Q. Zhou, F. Gao, J.W. Hagadorn, K.J. Peterson, and E.H. Davidson. 2000. Precambrian animal diversity: putative phosphatized embryos from the Doushantuo formation of China. Proceedings of the National Academy of Sciences of the United States of America 97: 4457–4462.

    Article  Google Scholar 

  • Chen, J.Y., D.J. Bottjer, E.H. Davidson, S.Q. Dornbos, X. Gao, Y.H. Yang, C.W. Li, G. Li, X.Q. Wang, D.C. Xian, H.J. Wu, Y.K. Hwu, and P. Tafforeau. 2006. Phosphatized polar lobe-forming embryos from the Precambrian of Southwest China. Science 312: 1644–1646.

    Article  Google Scholar 

  • Chen, J.Y., D.J. Bottjer, E.H. Davidson, G. Li, F. Gao, R.A. Cameron, M.G. Hadfield, D.C. Xian, P. Tafforeau, Q.J. Jia, H. Sugiyama, and R. Tang. 2009a. Phase contrast synchrotron X-ray microtomography of Ediacaran (Doushantuo) metazoan microfossils: Phylogenetic diversity and evolutionary implications. Precambrian Research 173: 191–200.

    Article  Google Scholar 

  • Chen, J.Y., D.J. Bottjer, G. Li, M.G. Hadfield, F. Gao, A.R. Cameron, C.Y. Zhang, D.C. Xian, P. Tafforeau, X. Liao, and Z.J. Yin. 2009b. Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng’an, Guizhou, China. Proceedings of the National Academy of Sciences of the United States of America 106: 19056–19060.

    Article  Google Scholar 

  • Chen, L., S.H. Xiao, K. Pang, C.M. Zhou, and X.L. Yuan. 2014. Cell differentiation and germ-soma separation in Ediacaran animal embryo-like fossils. Nature 516: 238–241.

    Article  Google Scholar 

  • Cunningham, J.A., C.W. Thomas, S. Bengtson, S.L. Kearns, S.H. Xiao, F. Marone, M. Stampanoni, and P.C.J. Donoghue. 2012a. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians. Proceedings of the Royal Society (B: Biological Sciences) 279: 2369–2376.

    Google Scholar 

  • Cunningham, J.A., C.W. Thomas, S. Bengtson, F. Marone, M. Stampanoni, F.R. Turner, J.V. Bailey, R.A. Raff, E.C. Raff, and P.C.J. Donoghue. 2012b. Experimental taphonomy of giant sulphur bacteria: Implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils. Proceedings of the Royal Society (B: Biological Sciences) 279: 1857–1864.

    Google Scholar 

  • Cunningham, J.A., K. Vargas, Z.J. Yin, S. Bengtson, and P.C.J. Donoghue. 2017. The Weng’an Biota (Doushantuo Formation): an Ediacaran window on soft-bodied and multicellular microorganisms. Journal of the Geological Society 174: 793–802.

    Article  Google Scholar 

  • Gostling, N.J., C.-W. Thomas, J.M. Greenwood, X.P. Dong, S. Bengtson, E.C. Raff, R.A. Raff, B.M. Degnan, M. Stampanoni, and P.C.J. Donoghue. 2008. Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy. Evoluiton and Development 10: 339–349.

    Article  Google Scholar 

  • Hagadorn, J.W., S.H. Xiao, P.C.J. Donoghue, S. Bengtson, N.J. Gostling, M. Pawlowska, E.C. Raff, R.A. Raff, F.R. Turner, C.Y. Yin, C.M. Zhou, X.L. Yuan, M.B. McFeely, M. Stampanoni, and K.H. Nealson. 2006. Cellular and subcellular structure of Neoproterozoic animal embryos. Science 314: 291–294.

    Article  Google Scholar 

  • Huldtgren, T., J.A. Cunningham, C.Y. Yin, M. Stampanoni, F. Marone, P.C.J. Donoghue, and S. Bengtson. 2011. Fossilized nuclei and germination structures identify Ediacaran “animal embryos” as encysting protists. Science 334: 1696–1699.

    Article  Google Scholar 

  • Pang, K., Q. Tang, J.D. Schiffbauer, J. Yao, X.L. Yuan, B. Wan, L. Chen, Z.J. Ou, and S.H. Xiao. 2013. The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11: 499–510.

    Google Scholar 

  • Raff, E.C., J.T. Villinski, F.R. Turner, P.C.J. Donoghue, and R.A. Raff. 2006. Experimental taphonomy shows the feasibility of fossil embryos. Proceedings of the National Academy of Sciences of the United States of America 103: 5846–5851.

    Article  Google Scholar 

  • Raff, E.C., K.L. Schollaert, D.E. Nelson, P.C.J. Donoghue, C.W. Thomas, F.R. Turner, B.D. Stein, X.P. Dong, S. Bengtson, and T. Huldtgren. 2008. Embryo fossilization is a biological process mediated by microbial biofilms. Proceedings of the National Academy of Sciences of the United States of America 105: 19360–19365.

    Article  Google Scholar 

  • Schiffbauer, J.D., S.H. Xiao, K. Sen Sharma, and G. Wang. 2012. The origin of intracellular structures in Ediacaran metazoan embryos. Geology 40: 223–226.

    Article  Google Scholar 

  • Sun, W.C., Z.J. Yin, J.A. Cunningham, P. Liu, M. Zhu, and P.C.J. Donoghue. 2020. Nucleus preservation in early Ediacaran Weng’an embryo-like fossils, experimental taphonomy of nuclei and implications for reading the eukaryote fossil record. Interface Focus 10: 20200015.

    Article  Google Scholar 

  • Xiao, S.H., and A.H. Knoll. 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstatte, South China. Lethaia 32: 219–240.

    Article  Google Scholar 

  • Xiao, S.H., and A.H. Knoll. 2000. Phosphatized animal embryos from the Neoproterozic Doushantuo Fomation at Weng’an, Guizhou, South China. Journal of Paleontology 74: 767–788.

    Article  Google Scholar 

  • Xiao, S.H., Y. Zhang, and A.H. Knoll. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391: 553–558.

    Article  Google Scholar 

  • Xiao, S.H., J.W. Hagadorn, C.M. Zhou, and X.L. Yuan. 2007a. Rare helical spheroidal fossils from the Doushantuo Lagerstatte: Ediacaran animal embryos come of age? Geology 35: 115–118.

    Article  Google Scholar 

  • Xiao, S.H., C.M. Zhou, and X.L. Yuan. 2007b. Palaeontology—undressing and redressing Ediacaran embryos. Nature 446: E9–E10.

    Article  Google Scholar 

  • Xiao, S.H., A.D. Muscente, L. Chen, C.M. Zhou, J.D. Schiffbauer, A.D. Wood, N.F. Polys, and X.L. Yuan. 2014a. The Weng’an biota and the Ediacaran radiation of multicellular eukaryotes. National Science Review 1: 498–520.

    Article  Google Scholar 

  • Xiao, S.H., C.M. Zhou, P.J. Liu, D. Wang, and X.L. Yuan. 2014b. Phosphatized Acanthomorphic Acritarchs and Related Microfossils from the Ediacaran Doushantuo formation at Weng’an (South China) and their implications for biostratigraphic correlation. Journal of Paleontology 88: 1–67.

    Article  Google Scholar 

  • Yin, Z.J., and M.Y. Zhu. 2012. New observations of the ornamented Doushantuo embryo fossils from the Ediacaran Weng’an Biota, South China. Bulletin of Geosciences 87: 171–181.

    Article  Google Scholar 

  • Yin, L.M., M.Y. Zhu, A.H. Knoll, X.L. Yuan, J.M. Zhang, and J. Hu. 2007. Doushantuo embryos preserved inside diapause egg cysts. Nature 446: 661–663.

    Article  Google Scholar 

  • Yin, Z.J., M.Y. Zhu, P. Tafforeau, J.Y. Chen, P.J. Liu, and G. Li. 2013. Early embryogenesis of potential bilaterian animals with polar lobe formation from the Ediacaran Weng’an Biota, South China. Precambrian Research 225: 44–57.

    Article  Google Scholar 

  • Yin, Z.J., M.Y. Zhu, D.J. Bottjer, F.C. Zhao, and P. Tafforeau. 2016. Meroblastic cleavage identifies some Ediacaran Doushantuo (China) embryo-like fossils as metazoans. Geology 44: 735–738.

    Article  Google Scholar 

  • Yin, Z.J., J.A. Cunningham, K. Vargas, S. Bengtson, M.Y. Zhu, and P.C.J. Donoghue. 2017. Nuclei and nucleoli in embryo-like fossils from the Ediacaran Weng’an Biota. Precambrian Research 301: 145–151.

    Article  Google Scholar 

  • Yin, Z.J., K. Vargas, J.A. Cunningham, S. Bengtson, M.Y. Zhu, F. Marone, and P.C.J. Donoghue. 2019. The early Ediacaran Caveasphaera Foreshadows the evolutionary origin of animal-like embryology. Current Biology 29: 4307–4314.

    Article  Google Scholar 

  • Yin, Z.J., W.C. Sun, P.J. Liu, M.Y. Zhu, and P.C.J. Donoghue. 2020. Developmental biology of Helicoforamina reveals holozoan affinity, cryptic diversity, and adaptation to heterogeneous environments in the early Ediacaran Weng’an biota (Doushantuo Formation, South China). Science Advances 6: eabb0083.

    Article  Google Scholar 

  • Zhang, X.G., and B.R. Pratt. 2014. Possible algal origin and life cycle of ediacaran doushantuo microfossils with dextral spiral structure. Journal of Paleontology 88: 92–98.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Suping Wu and Yan Fang from the Experimental Technologies Center of NIGPAS for their help in tomographic reconstruction and EDS elemental mapping. We also would like to thank Lixin Gu from the Electron Microscopy Laboratory of IGGCAS, Shukang Zhang from IVPP and Yanhong Pan from Nanjing University for their helps in sample preparation. This research is supported by Strategic Priority Research Program (B) of the Chinese Academy of Sciences (CAS) (XDB26000000), the National Natural Science Foundation of China (42022010, 41921002), CAS Interdisciplinary Innovation Team (JCTD-2020-18), and the Youth Innovation Promotion Association of the CAS. In addition, Zongjun Yin, Philip Donoghue and Maoyan Zhu were funded by Natural Environment Research Council (NERC) grant (NE/P013678/1), part of the Biosphere Evolution, Transitions and Resilience (BETR) programme, which is co-funded by the Natural Science Foundation of China (NSFC).

Author information

Authors and Affiliations

  1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, 210008, China

    Weichen Sun, Zongjun Yin & Maoyan Zhu

  2. Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, 210008, China

    Weichen Sun, Zongjun Yin & Maoyan Zhu

  3. University of Science and Technology of China, Hefei, 230026, China

    Weichen Sun

  4. Institute of Geology, Chinese Academy of Geological Sciences, Beijing, 100043, China

    Pengju Liu

  5. School of Earth Sciences, Life Sciences Building, University of Bristol, Tyndall Avenue, Bristol, BS8 1TQ, UK

    Philip C. J. Donoghue

  6. Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Innovation Academy for Earth Science, Chinese Academy of Sciences, Beijing, 100029, China

    Jinhua Li

  7. College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China

    Zongjun Yin & Maoyan Zhu

Authors
  1. Weichen Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zongjun Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pengju Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip C. J. Donoghue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinhua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maoyan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zongjun Yin.

Additional information

Handling Editor: Joachim Reitner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, W., Yin, Z., Liu, P. et al. Ultrastructure and in-situ chemical characterization of intracellular granules of embryo-like fossils from the early Ediacaran Weng’an biota. PalZ 95, 611–621 (2021). https://doi.org/10.1007/s12542-021-00597-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12542-021-00597-0

Keywords

Search

Navigation