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Algal origin of sponge sterane biomarkers negates the oldest evidence for animals in the rock record

Nature Ecology & Evolution volume 5, pages 165–168 (2021)Cite this article

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Abstract

The earliest fossils of animal-like organisms occur in Ediacaran rocks that are approximately 571 million years old. Yet 24-isopropylcholestanes and other C30 fossil sterol molecules have been suggested to reflect an important ecological role of demosponges as the first abundant animals by the end of the Cryogenian period (>635 million years ago). Here, we demonstrate that C30 24-isopropylcholestane is not diagnostic for sponges and probably formed in Neoproterozoic sediments through the geological methylation of C29 sterols of chlorophyte algae, the dominant eukaryotes at that time. These findings reconcile biomarker evidence with the geological record and revert the oldest evidence for animals back into the latest Ediacaran.

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Fig. 1: Distribution of C30 steranes in the rock record and in the pyrolysis/hydrogenation products from algal sterols.

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All data that support the paper are presented in the main text of the manuscript and in the Supplementary Information.

References

  1. Fedonkin, M. A., Simonetta, A. & Ivantsov, A. Y. New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. Geol. Soc. Spec. Publ. 286, 157–179 (2007).

    Article  Google Scholar 

  2. Xiao, S. & Laflamme, M. On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol. Evol. 24, 31–40 (2009).

    Article  PubMed  Google Scholar 

  3. Budd, G. E. & Jensen, S. The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution. Biol. Rev. 92, 446–473 (2017).

    Article  PubMed  Google Scholar 

  4. Bobrovskiy, I. et al. Ancient steroids establish the Ediacaran fossil Dickinsonia as one of the earliest animals. Science 361, 1246–1249 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Dunn, F. S., Liu, A. G. & Donoghue, P. C. Ediacaran developmental biology. Biol. Rev. 93, 914–932 (2018).

    Article  PubMed  Google Scholar 

  6. Parfrey, L. W., Lahr, D. J., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. Dos Reis, M. et al. Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Curr. Biol. 25, 2939–2950 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Dohrmann, M. & Wörheide, G. Dating early animal evolution using phylogenomic data. Sci. Rep. 7, 3599 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Lozano-Fernandez, J., dos Reis, M., Donoghue, P. C. J. & Pisani, D. RelTime rates collapse to a strict clock when estimating the timeline of animal diversification. Genome Biol. Evol. 9, 1320–1328 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Cunningham, J. A., Liu, A. G., Bengtson, S. & Donoghue, P. C. The origin of animals: can molecular clocks and the fossil record be reconciled?. Bioessays 39, 1600120 (2017).

    Article  Google Scholar 

  12. Budd, G. E. & Mann, R. P. The dynamics of stem and crown groups. Sci. Adv. 6, eaaz1626 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Brocks, J. J. & Pearson, A. Building the biomarker tree of life. Rev. Mineral. Geochem. 59, 233–258 (2005).

    Article  CAS  Google Scholar 

  14. Volkman, J. K. Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways. Org. Geochem. 36, 139–159 (2005).

    Article  CAS  Google Scholar 

  15. Zumberge, J. A. A Lipid Biomarker Investigation Tracking the Evolution of the Neoproterozoic Marine Biosphere and the Rise of Eukaryotes. PhD thesis, Univ. California Riverside (2019); https://escholarship.org/uc/item/86p25344

  16. McCaffrey, M. A. et al. Paleoenvironmental implications of novel C30 steranes in Precambrian to Cenozoic age petroleum and bitumen. Geochim. Cosmochim. Acta 58, 529–532 (1994).

    Article  CAS  Google Scholar 

  17. Zumberge, J. A. et al. Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals. Nat. Ecol. Evol. 2, 1709–1714 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009).

    Article  CAS  PubMed  Google Scholar 

  19. Love, G. D. et al. Sources of C30 steroid biomarkers in Neoproterozoic–Cambrian rocks and oils. Nat. Ecol. Evol. 4, 34–36 (2020).

    Article  PubMed  Google Scholar 

  20. Gold, D. A. et al. Sterol and genomic analyses validate the sponge biomarker hypothesis. Proc. Natl Acad. Sci. USA 113, 2684–2689 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Nettersheim, B. J. et al. Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals. Nat. Ecol. Evol. 3, 577–581 (2019).

    Article  PubMed  Google Scholar 

  22. Botting, J. P. & Muir, L. A. Early sponge evolution: a review and phylogenetic framework. Palaeoworld 27, 1–29 (2018).

    Article  Google Scholar 

  23. Botting, J. P. & Nettersheim, B. J. Searching for sponge origins. Nat. Ecol. Evol. 2, 1685–1686 (2018).

    Article  PubMed  Google Scholar 

  24. Antcliffe, J. B. Questioning the evidence of organic compounds called sponge biomarkers. Palaeontology 56, 917–925 (2013).

    Google Scholar 

  25. Grosjean, E. et al. Origin of petroleum in the Neoproterozoic–Cambrian South Oman salt basin. Org. Geochem. 40, 87–110 (2009).

    Article  CAS  Google Scholar 

  26. Stolper, D. et al. Paleoecology and paleoceanography of the Athel silicilyte, Ediacaran-Cambrian boundary, Sultanate of Oman. Geobiology 15, 401–426 (2017).

    Article  CAS  PubMed  Google Scholar 

  27. Bhattacharya, S. & Dutta, S. Neoproterozoic-Early Cambrian biota and ancient niche: a synthesis from molecular markers and palynomorphs from Bikaner-Nagaur Basin, western India. Precambrian Res. 266, 361–374 (2015).

    Article  CAS  Google Scholar 

  28. Mills, D. B. et al. Oxygen requirements of the earliest animals. Proc. Natl Acad. Sci. USA 111, 4168–4172 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. van Maldegem, L. M. et al. Bisnorgammacerane traces predatory pressure and the persistent rise of algal ecosystems after Snowball Earth. Nat. Commun. 10, 476 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Hallmann, C. et al. Reply to: Sources of C30 steroid biomarkers in Neoproterozoic–Cambrian rocks and oils. Nat. Ecol. Evol. 4, 37–39 (2020).

    Article  PubMed  Google Scholar 

  31. Love, G. D. & Summons, R. E. The molecular record of Cryogenian sponges – a response to Antcliffe (2013). Palaeontology 58, 1131–1136 (2015).

    Article  Google Scholar 

  32. Brocks, J. J. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017).

    Article  CAS  PubMed  Google Scholar 

  33. Hoshino, Y. et al. Cryogenian evolution of stigmasteroid biosynthesis. Sci. Adv. 3, e1700887 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Bobrovskiy, I., Hope, J. M., Golubkova, E. & Brocks, J. J. Food sources for the Ediacara biota communities. Nat. Commun. 11, 1261 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Silberfeld, T. et al. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”. Mol. Phylogenet. Evol. 56, 659–674 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Knoll, A. H., Summons, R. E., Waldbauer, J. R. & Zumberge, J. E. in Evolution of Primary Producers in the Sea (eds Falkowski, P. & Knoll, A. H.) Ch. 8 (Elsevier Acad. Press, 2007).

  37. Kodner, R. B., Pearson, A., Summons, R. E. & Knoll, A. H. Sterols in red and green algae: quantification, phylogeny, and relevance for the interpretation of geologic steranes. Geobiology 6, 411–420 (2008).

    Article  CAS  PubMed  Google Scholar 

  38. Summons, R. E. & Capon, R. J. Identification and significance of 3β-ethyl steranes in sediments and petroleum. Geochim. Cosmochim. Acta 55, 2391–2395 (1991).

    Article  CAS  Google Scholar 

  39. Dahl, J. et al. Extended 3β-alkyl steranes and 3-alkyl triaromatic steroids in crude oils and rock extracts. Geochim. Cosmochim. Acta 59, 3717–3729 (1995).

    Article  CAS  Google Scholar 

  40. Kissin, Y. V. Catagenesis and composition of petroleum: origin of n-alkanes and isoalkanes in petroleum crudes. Geochim. Cosmochim. Acta 51, 2445–2457 (1987).

    Article  CAS  Google Scholar 

  41. Rushdi, A. I., Ritter, G., Grimalt, J. O. & Simoneit, B. R. T. Hydrous pyrolysis of cholesterol under various conditions. Org. Geochem. 34, 799–812 (2003).

    Article  CAS  Google Scholar 

  42. Koopmans, M. P. et al. Diagenetic and catagenetic products of isorenieratene: molecular indicators for photic zone anoxia. Geochim. Cosmochim. Acta 60, 4467–4496 (1996).

    Article  CAS  Google Scholar 

  43. Alexander, R., Berwick, L. & Pierce, K. Single carbon surface reactions of 1-octadecene and 2,3,6-trimethylphenol on activated carbon: implications for methane formation in sediments. Org. Geochem. 42, 540–547 (2011).

    Article  CAS  Google Scholar 

  44. Volkman, J. K., Barrett, S. M., Dunstan, G. A. & Jeffrey, S. Sterol biomarkers for microalgae from the green algal class Prasinophyceae. Org. Geochem. 21, 1211–1218 (1994).

    Article  CAS  Google Scholar 

  45. van Maldegem, L. M. et al. Geological alteration of Precambrian steroids mimics early animal signatures. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-020-01336-5 (2020).

  46. Brocks, J. J. & Hope, J. M. Tailing of chromatographic peaks in GC-MS caused by interaction of halogenated solvents with the ion source. J. Chromatogr. Sci. 52, 471–475 (2014).

    Article  CAS  PubMed  Google Scholar 

  47. Peters, K. E., Walters, C. C. & Moldowan, J. M. The Biomarker Guide. Biomarkers and Isotopes in Petroleum Systems and Earth History 2nd edn, Vol. 2 (Cambridge Univ. Press, 2005).

Download references

Acknowledgements

The study was funded by the Australian Research Council grants DP160100607 and DP170100556 (to J.J.B.). I.B. gratefully acknowledges the Texaco Postdoctoral Fellowship. The authors are grateful to L. M. van Maldegem, P. Adam and P. Schaeffer for their helpful feedback.

Author information

Authors and Affiliations

  1. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA

    Ilya Bobrovskiy

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

    Ilya Bobrovskiy, Janet M. Hope & Jochen J. Brocks

  3. Max Planck Institute for Biogeochemistry, Jena, Germany

    Benjamin J. Nettersheim & Christian Hallmann

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

    Benjamin J. Nettersheim & Christian Hallmann

  5. CSIRO Oceans and Atmosphere, Hobart, Tasmania, Australia

    John K. Volkman

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Contributions

I.B. conceived the study, performed the analyses and wrote the first draft. J.M.H. and J.K.V. helped with compound identification. I.B. and B.J.N. interpreted the data. I.B., J.M.H., B.J.N., J.K.V., C.H. and J.J.B. prepared the manuscript.

Corresponding authors

Correspondence to Ilya Bobrovskiy or Jochen J. Brocks.

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Extended data

Extended Data Fig. 1 Mass spectra of steranes produced via pyrolysis of (iso)fucosterol and saringosterol.

All mass spectra presented in this figure were obtained from one of the S. fusiforme pyrolysates; it was not possible to obtain a pure mass spectrum for βαα 24-npc due to coelution with other compounds.

Supplementary information

Supplementary Information

Supplementary Discussion, Tables 2–4 and references.

Reporting Summary

Supplementary Table 1

Sterol composition of green algae reported in the literature.

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Bobrovskiy, I., Hope, J.M., Nettersheim, B.J. et al. Algal origin of sponge sterane biomarkers negates the oldest evidence for animals in the rock record. Nat Ecol Evol 5, 165–168 (2021). https://doi.org/10.1038/s41559-020-01334-7

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  • DOI: https://doi.org/10.1038/s41559-020-01334-7

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