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Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

Nature Ecology & Evolution volume 2, pages 1709–1714 (2018)Cite this article

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Abstract

Sterane biomarkers preserved in ancient sedimentary rocks hold promise for tracking the diversification and ecological expansion of eukaryotes. The earliest proposed animal biomarkers from demosponges (Demospongiae) are recorded in a sequence around 100 Myr long of Neoproterozoic–Cambrian marine sedimentary strata from the Huqf Supergroup, South Oman Salt Basin. This C30 sterane biomarker, informally known as 24-isopropylcholestane (24-ipc), possesses the same carbon skeleton as sterols found in some modern-day demosponges. However, this evidence is controversial because 24-ipc is not exclusive to demosponges since 24-ipc sterols are found in trace amounts in some pelagophyte algae. Here, we report a new fossil sterane biomarker that co-occurs with 24-ipc in a suite of late Neoproterozoic–Cambrian sedimentary rocks and oils, which possesses a rare hydrocarbon skeleton that is uniquely found within extant demosponge taxa. This sterane is informally designated as 26-methylstigmastane (26-mes), reflecting the very unusual methylation at the terminus of the steroid side chain. It is the first animal-specific sterane marker detected in the geological record that can be unambiguously linked to precursor sterols only reported from extant demosponges. These new findings strongly suggest that demosponges, and hence multicellular animals, were prominent in some late Neoproterozoic marine environments at least extending back to the Cryogenian period.

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Fig. 1: MRM-GC-MS ion chromatograms of C30 sterane distributions (414 → 217 Da ion transitions).
Fig. 2: Chemical structures of stelliferasterol, isostelliferasterol and strongylosterol.
Fig. 3: A revised Neoproterozoic–Cambrian timeline showing co-occurrences of 26-mes and 24-ipc sterane biomarkers.
Fig. 4: Chemical structures for a selection of conventional, unconventional and unsaturated sterols found in modern eukaryotic taxa.

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The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files.

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Acknowledgements

Funding support for this work came from the NASA Astrobiology Institute teams Alternative Earths (NNA15BB03A) and Foundations of Complex Life (NNA13AA90A), NASA Exobiology program (grant number 80NSSC18K1085), NSF Frontiers in Earth System Dynamics programme (grant number 1338810), Agouron Institute, and European Union’s Horizon 2020 research and innovation programme through the SponGES project (grant agreement number 679849). Many thanks go to the sponge collectors, including T. Pérez, H. Tore Rapp, A. Plotkin, J.-S. Hong, Y. M. Huang, S. Rohde, S. Nichols, J. V. Lopez, B. Calcinai, G. Gatti, B. Ciperling, J. Boavida, J.-P. Fonseca, L. Magro and F. Azzini. The fieldwork on the Mohns and Knipovich Ridges aboard the RV G. O. Sars in 2014 was supported by the Research Council of Norway through the Centre for Geobiology, UiB (contract number 179560). A Vazella pourtalesii specimen was provided by E. Kenchington through funding from the Marine Conservation Target fund of the Department of Fisheries and Oceans Canada. Other specimens were provided by E. Kenchington as Canadian lead for the NEREIDA (NAFO Potential Vulnerable Marine Ecosystems-Impacts of Deep-sea Fisheries) project led by Spain and Canada. We thank K. Ubhayasekera (Department of Chemistry, Uppsala University) for GC-MS analyses, and S. Rajendran and T. Aljazar (Department of Medicinal Chemistry, Uppsala University) for help with the isolation of sponge sterols. We thank Petroleum Development Oman for Neoproterozoic–Cambrian rock samples from the South Oman Salt Basin for ancient biomarker analysis. We are grateful to D. Rocher for GC-QQQ-MS analysis and GeoMark Research (Houston, TX) for providing oil samples from Eastern Siberia.

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Authors and Affiliations

  1. Department of Earth Sciences, University of California, Riverside, Riverside, CA, USA

    J. Alex Zumberge & Gordon D. Love

  2. Department of Medicinal Chemistry, Uppsala University, Uppsala, Sweden

    Paco Cárdenas & Sunithi Gunasekera

  3. Department of Geological Sciences, Stanford University, Stanford, CA, USA

    Erik A. Sperling

  4. Department of Earth and Atmospheric Sciences, Central Michigan University, Mount Pleasant, MI, USA

    Megan Rohrssen

  5. Geoscience Australia, Canberra, Australian Capital Territory, Australia

    Emmanuelle Grosjean

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

    John P. Grotzinger

  7. Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    Roger E. Summons

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Contributions

J.A.Z. and G.D.L. planned the investigation and wrote the manuscript with input from P.C. and E.A.S. J.A.Z. processed and interpreted the lipid biomarker data with help from G.D.L., E.G., R.E.S. and M.R. P.C., E.A.S., R.E.S., S.G., M.R., E.G. and J.P.G. provided comments on drafts of the manuscript.

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Correspondence to Gordon D. Love.

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Supplementary information

Supplementary Information

Supplementary methods, figures 1–6, tables 2–4; 6, chart

Reporting Summary

Supplementary Table 1

Selected biomarker ratios and yields obtained from free saturate fractions of sediment cores and cuttings from South Oman Salt Basin

Supplementary Table 5

C30 regular (4-desmethyl) sterane patterns from catalytic hydropyrolysis (HyPy) of the modern sponges used in this study

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Zumberge, J.A., Love, G.D., Cárdenas, P. et al. Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals. Nat Ecol Evol 2, 1709–1714 (2018). https://doi.org/10.1038/s41559-018-0676-2

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