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Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals

Nature Ecology & Evolution volume 3, pages 577–581 (2019)Cite this article

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Matters Arising to this article was published on 25 November 2019

Abstract

The dawn of animals remains one of the most mysterious milestones in the evolution of life. The fossil lipids 24-isopropylcholestane and 26-methylstigmastane are considered diagnostic for demosponges—arguably the oldest group of living animals. The widespread occurrence and high relative abundance of these biomarkers in Ediacaran sediments from 635–541 million years (Myr) ago have been viewed as evidence for the rise of animals to ecological importance approximately 100 Myr before their rapid Cambrian radiation. Here we show that the biosynthesis of 24-isopropylcholestane and 26-methylstigmastane precursors is common among early-branching unicellular Rhizaria—heterotrophic protists that play an important role in trophic cycling and carbon export in the modern ocean. Negating these hydrocarbons as sponge biomarkers, our study places the oldest evidence for animals closer to the Cambrian Explosion. Cambrian silica hexactine spicules that are approximately 535 Myr old now represent the oldest diagnostic sponge remains, whereas approximately 558-Myr-old Dickinsonia and Kimberella (Ediacara biota) provide the most reliable evidence for the emergence of animals. The proliferation of predatory protists may have been responsible for much of the ecological changes during the late Neoproterozoic, including the rise of algae, the establishment of complex trophic relationships and the oxygenation of shallow-water habitats required for the subsequent ascent of macroscopic animals.

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Fig. 1: Geological evidence for Metazoa and Rhizaria.
Fig. 2: C30 steroids in Rhizaria.

Data availability

The data required to assess the interpretations made in this paper are included in the Supplementary Information. Additional (raw) data are available from the corresponding authors upon reasonable request.

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Acknowledgements

We thank P. Pringle and R. Tarozo for laboratory support; A. Leider, Y. Hoshino, M. Neumann, N. Kuznetsov and L. van Maldegem for discussions and reference samples; M. Holzmann, R. Sierra, J. Bernhard, S. Eggins, C. Bachy and C. Reymond for assistance in sourcing specimens; and S. Porter, R. Meisterfeld, S. Pruss, S. Chang and J. Botting for fossil images. This study was principally funded by the Max Planck Society (to C.H. and R.S.) and the Agouron Institute (Geobiology fellowship to B.J.N.). We also acknowledge the US National Science Foundation (grant nos. PLR134161 to S.S.B. and DBI-1349350 to M.W.L.), Swiss National Science Foundation (grant no. 31003A_179125 to J.P.), the German Research Foundation (grant no. NO1090/1-1 to E.N.), the Leibniz Association (grant no. SAW-2014-ISAS-2 to M.S.), Formas, the Swedish Research Council (A.S.), the French National Research Agency (grant no. IMPEKAB ANR-15-CE02-001 to F.N.) and Australian Research Council (grant nos. DP1095247 and DP160100607 to J.J.B.).

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Authors and Affiliations

  1. Max Planck Institute for Biogeochemistry, Jena, Germany

    Benjamin J. Nettersheim & Christian Hallmann

  2. MARUM—Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany

    Benjamin J. Nettersheim, Christiane Schmidt, Karin Zonneveld, Michal Kucera & Christian Hallmann

  3. Research School of Earth Sciences, The Australian National University, Canberra, Australian Capital Territory, Australia

    Jochen J. Brocks, Janet M. Hope, Patrick De Deckker & Ilya Bobrovskiy

  4. Department of Plant Biology, Uppsala BioCentre Linnean Centre for Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Arne Schwelm

  5. Institute of Microbiology, University of Innsbruck, Innsbruck, Austria

    Arne Schwelm

  6. Adaptation and Diversity in Marine Environment (AD2M), Laboratory Ecology of Marine Plankton team Station Biologique de Roscoff, Sorbonne Université, CNRS, UMR7144, Roscoff, France

    Fabrice Not

  7. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA

    Michael Lomas

  8. Max Planck Institute for Chemistry, Mainz, Germany

    Ralf Schiebel

  9. Department of Biology, Heinrich-Heine-Universität Düsseldorf, Dusseldorf, Germany

    Eva C. M. Nowack

  10. Department of Genetics and Evolution, University of Geneva, Geneva, Switzerland

    Jan Pawlowski

  11. Wadsworth Center, New York State Department of Health, Albany, NY, USA

    Samuel S. Bowser

  12. Leibniz Centre for Tropical Marine Research (ZMT), Biogeochemistry and Geology, Bremen, Germany

    Marleen Stuhr

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  1. Benjamin J. Nettersheim
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Contributions

B.J.N., C.H. and J.J.B. designed the study. A.S., F.N., M.L., C.S., R.S., E.C.M.N., P.D.D., J.P., S.S.B., K.Z. and M.S. cultured, collected and provided specimens. J.M.H. analysed Acantharea and I.B. analysed fossil algae. B.J.N. collected some specimens and analysed all other samples. B.J.N. and C.H. analysed and interpreted data. B.J.N., C.H. and J.J.B. wrote the manuscript with input from all authors.

Corresponding authors

Correspondence to Benjamin J. Nettersheim or Christian Hallmann.

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Supplementary Figures 1–8, Supplementary Tables 1 and 2, Supplementary Methods and Supplementary Text

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Nettersheim, B.J., Brocks, J.J., Schwelm, A. et al. Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals. Nat Ecol Evol 3, 577–581 (2019). https://doi.org/10.1038/s41559-019-0806-5

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