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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.

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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.

References

  1. Lenton, T. M., Boyle, R. A., Poulton, S. W., Shields-Zhou, G. A. & Butterfield, N. J. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).

    Article  CAS  Google Scholar 

  2. Butterfield, N. J. The Neoproterozoic. Curr. Biol. 25, R859–R863 (2015).

    Article  CAS  Google Scholar 

  3. Antcliffe, J. B., Callow, R. H. & Brasier, M. D. Giving the early fossil record of sponges a squeeze. Biol. Rev. 89, 972–1004 (2014).

    Article  Google Scholar 

  4. Botting, J. P. & Muir, L. A. Early sponge evolution: a review and phylogenetic framework. Palaeoworld 27, 1–29 (2017).

  5. 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  Google Scholar 

  6. Peterson, K. J. et al. Estimating metazoan divergence times with a molecular clock. Proc. Natl Acad. Sci. USA 101, 6536–6541 (2004).

    Article  CAS  Google Scholar 

  7. 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  Google Scholar 

  8. Hedges, S. B., Blair, J. E., Venturi, M. L. & Shoe, J. L. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4, 2 (2004).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Grosjean, E., Love, G., Stalvies, C., Fike, D. & Summons, R. Origin of petroleum in the Neoproterozoic–Cambrian South Oman salt basin. Org. Geochem. 40, 87–110 (2009).

    Article  CAS  Google Scholar 

  13. 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  Google Scholar 

  14. Grabenstatter, J. et al. Identification of 24-n-propylidenecholesterol in a member of the Foraminifera. Org. Geochem. 63, 145–151 (2013).

    Article  CAS  Google Scholar 

  15. Sierra, R. et al. Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel’s Radiolaria. Mol. Phylogenet. Evol. 67, 53–59 (2013).

    Article  Google Scholar 

  16. Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465–470 (2016).

    Article  CAS  Google Scholar 

  17. Porter, S. M., Meisterfeld, R. & Knoll, A. H. Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae. J. Paleontol. 77, 409–429 (2003).

    Article  Google Scholar 

  18. Bosak, T. et al. Possible early foraminiferans in post-Sturtian (716−635 Ma) cap carbonates. Geology 40, 67–70 (2012).

    Article  CAS  Google Scholar 

  19. Pawlowski, J. et al. The evolution of early Foraminifera. Proc. Natl Acad. Sci. USA 100, 11494–11498 (2003).

    Article  CAS  Google Scholar 

  20. Groussin, M., Pawlowski, J. & Yang, Z. Bayesian relaxed clock estimation of divergence times in foraminifera. Mol. Phylogenet. Evol. 61, 157–166 (2011).

    Article  Google Scholar 

  21. Caron, D. A. The rise of Rhizaria. Nature 532, 444–445 (2016).

    Article  CAS  Google Scholar 

  22. Lampitt, R. S., Salter, I. & Johns, D. Radiolaria: major exporters of organic carbon to the deep ocean. Glob. Biogeochem. Cycles 23, GB1010 (2009).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Sperling, E., Robinson, J., Pisani, D. & Peterson, K. Where’s the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200‐Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology 8, 24–36 (2010).

    Article  CAS  Google Scholar 

  25. Gold, D. A., O’Reilly, S. S., Luo, G., Briggs, D. E. G. & Summons, R. E. Prospects for sterane preservation in sponge fossils from museum collections and the utility of sponge biomarkers for molecular clocks. Bull. Peabody Mus. Nat. Hist. 57, 181–189 (2016).

    Article  Google Scholar 

  26. Katz, M. E., Fennel, K. & Falkowski, P. G. in Evolution of Primary Producers in the Sea 405–430 (Elsevier, Amsterdam, 2007).

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

    Article  Google Scholar 

  28. 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  Google Scholar 

  29. Volkman, J. Sterols in microorganisms. Appl. Microbiol. Biotechnol. 60, 495–506 (2003).

    Article  CAS  Google Scholar 

  30. Bobrovskiy, I., Hope, J. M., Krasnova, A., Ivantsov, A. & Brocks, J. J. Molecular fossils from organically preserved Ediacara biota reveal cyanobacterial origin for Beltanelliformis. Nat. Ecol. Evol. 2, 437–440 (2018).

    Article  Google Scholar 

  31. Brocks, J. J. et al. Early sponges and toxic protists: possible sources of cryostane, an age diagnostic biomarker antedating Sturtian Snowball Earth. Geobiology 14, 129–149 (2016).

    Article  CAS  Google Scholar 

  32. Lenton, T. M. & Daines, S. J. The effects of marine eukaryote evolution on phosphorus, carbon and oxygen cycling across the Proterozoic–Phanerozoic transition. Emerg. Top. Life. Sci. 2, 267–278 (2018).

    Article  CAS  Google Scholar 

  33. Jürgens, K. & Massana, R. in Microbial Ecology of the Oceans 2nd edn (ed. Kirchman, D.) 383–442 (Wiley–Blackwell, Hoboken, NJ, USA, 2008).

  34. Boraas, M. E., Seale, D. B. & Boxhorn, J. E. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evol. Ecol. 12, 153–164 (1998).

    Article  Google Scholar 

  35. Grazhdankin, D. Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution. Paleobiology 30, 203–221 (2004).

    Article  Google Scholar 

  36. 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, 1–12 (2017).

    Article  Google Scholar 

  37. Chang, S., Feng, Q., Clausen, S. & Zhang, L. Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: the earliest biomineralizing sponge record. Palaeogeogr. Palaeoclimatol. Palaeoecol. 474, 36–44 (2017).

    Article  Google Scholar 

  38. Botting, J. P., Cárdenas, P. & Peel, J. S. A crown-group demosponge from the early Cambrian Sirius Passet biota, North Greenland. Palaeontology 58, 35–43 (2015).

    Article  Google Scholar 

  39. Peters, K. E., Walters, C. C. & Moldowan, J. M. The Biomarker Guide. Volume 2: Biomarkers and Isotopes in Petroleum Exploration and Earth History (Cambridge Univ. Press, New York, 2005).

  40. Hallmann, C., Kelly, A. E., Gupta, S. N. & Summons, R. E. in Quantifying the Evolution of Early Life 355–401 (Springer, Dordrecht, the Netherlands, 2011).

  41. French, K. L. et al. Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc. Natl Acad. Sci. USA 112, 5915–5920 (2015).

    Article  CAS  Google Scholar 

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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.

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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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