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The rise of algae in Cryogenian oceans and the emergence of animals

Nature volume 548, pages 578–581 (2017)Cite this article

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Abstract

The transition from dominant bacterial to eukaryotic marine primary productivity was one of the most profound ecological revolutions in the Earth’s history, reorganizing the distribution of carbon and nutrients in the water column and increasing energy flow to higher trophic levels. But the causes and geological timing of this transition, as well as possible links with rising atmospheric oxygen levels1 and the evolution of animals2, remain obscure. Here we present a molecular fossil record of eukaryotic steroids demonstrating that bacteria were the only notable primary producers in the oceans before the Cryogenian period (720–635 million years ago). Increasing steroid diversity and abundance marks the rapid rise of marine planktonic algae (Archaeplastida) in the narrow time interval between the Sturtian and Marinoan ‘snowball Earth’ glaciations, 659–645 million years ago. We propose that the incumbency of cyanobacteria was broken by a surge of nutrients supplied by the Sturtian deglaciation3. The ‘Rise of Algae’ created food webs with more efficient nutrient and energy transfers4, driving ecosystems towards larger and increasingly complex organisms. This effect is recorded by the concomitant appearance of biomarkers for sponges5 and predatory rhizarians, and the subsequent radiation of eumetazoans in the Ediacaran period2.

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Figure 1: Time chart from 850 Myr ago to the present summarizing environmental, biomarker and fossil data and highlighting the position of the rise of algae.

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Acknowledgements

Funding support for this work came from Australian Research Council (ARC) grants DP0557499, DP1095247, DP160100607 and DP170100556. We thank the Geological Survey of Western Australia (GSWA), the Northern Territory Geological Survey (NTGS), and S. Porter and M. Moczydłowska for access to samples. J. M. Hope provided technical assistance, including the maintenance of mass spectrometers at The Australian National University.

Author information

Author notes

  1. Yosuke Hoshino

    Present address: School of Biological Sciences, Georgia Institute of Technology, Atlanta, 310 Ferst Drive NW, Georgia, 30322, USA

Authors and Affiliations

  1. Research School of Earth Sciences, The Australian National University, Canberra, 2601, Australian Capital Territory, Australia

    Jochen J. Brocks, Amber J. M. Jarrett, Eva Sirantoine & Tharika Liyanage

  2. Max Planck Institute for Biogeochemistry, Hans-Knoell-Straße 10, Jena, 07745, Germany

    Christian Hallmann & Yosuke Hoshino

  3. MARUM—Center for Marine Environmental Sciences, University of Bremen, Leobener Straße 8, 28359 Bremen, Germany

    Christian Hallmann

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Contributions

J.J.B. conceived the project and processed and interpreted the data. A.J.M.J. analysed and interpreted all biomarkers from the Amadeus Basin and Chuar Group. E.S. analysed biomarkers from the Western Officer Basin and Visingsö Group. T.L. collated data from the Ediacaran and Phanerozoic, and processed Tonian biomarker data. J.J.B. wrote the paper with contributions from C.H. and Y.H.

Corresponding author

Correspondence to Jochen J. Brocks.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks N. Planavsky, J. Sepúlveda and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Cryogenian Aralka Formation with a Phanerozoic oil.

Aralka sample 13J903 (drillcore BR05; 480.45 m) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes. d, C27 steranes.

Extended Data Figure 2 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Tonian Steptoe Formation with a Phanerozoic oil.

Steptoe sample 14B213 (drillcore Empress-1A; 588.21 m) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes. d, C27 steranes.

Extended Data Figure 3 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Kanpa Formation with a Phanerozoic oil.

Kanpa sample 14B211 (drillcore Empress-1A; 830.35 m) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes, highlighting the presence of indigenous ergostane (erg) and cryostane (cryo). d, C27 steranes.

Extended Data Figure 4 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Chuar Group with a Phanerozoic oil.

Outcrop sample 10J092 (1,494 m above base of Chuar Group) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes, highlighting the presence of indigenous cryostane but the absence of ergostane; d, C27 steranes.

Extended Data Figure 5 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Wallara Formation with a Phanerozoic oil.

Wallara sample 11J021 (drillcore BR05; 573.06 m) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes. d, C27 steranes.

Extended Data Figure 6 MRM chromatograms of M+ → 217 precursor–product transitions contrasting the sterane distribution of the Johnnys Creek Formation with a Phanerozoic oil.

Johnnys Creek sample 11J024 (drillcore BR05; 816.26 m) denoted by coloured traces; the AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, C30 steranes. b, C29 steranes. c, C28 steranes. d, C27 steranes.

Extended Data Figure 7 MRM chromatograms comparing C30 and C28 sterane distributions of the Chuar Group (sample 10J092) with a Phanerozoic oil.

AGSO-II industrial standard (a mixture of representative Phanerozoic oils) denoted by grey traces. a, m/z 414 → 217 traces of several Chuar Group samples contain chromatographic peaks with a typical C30 sterane elution pattern. However, elution times are considerably shifted towards the right relative to 24-n-propylcholestane (24-npc) or 24-isopropylcholestane (not shown). The compound may be a homologue of cryostane, but the structure remains unknown. b, Elution behaviour of cryostane in comparison to ergostane. The chromatograms are characterized by MRM M+ → 217 precursor–product transitions.

Extended Data Figure 8 m/z 231 mass chromatograms showing the distribution of triaromatic steroids in Tonian formations.

Insets are magnifications of the main trace to highlight the absence or presence of triaromatic ergosteroids and stigmasteroids. Chol, triaromatic cholesteroid (violet); Erg, triaromatic ergosteroid (blue); Stig, triaromatic stigmasteroid (green). a, Steptoe Fm. 14B213 (Empress-1A, 588.21 m) shows clear cholesteroid signals while ergosteroids and stigmasteroids are below detection limits. b, Kanpa Fm. 12B212 (Empress-1A, 629.60 m). c, Kanpa Fm. (12B204, Empress-1A, 830.35 m) showing triaromatic cholesteroids as well as ergosteroids but an absence of stigmasteroids (the first small peak in the elution position of 20S stigmasteroid is a different compound—this is highlighted by the absence of the 20R isomer, which should also always be present). d, Hussar Fm. 14B202 (Empress-1A, 1072.85 m). e, Chuar Group 10J093 (outcrop, 1,544.2 m above base of group). f, Visingsö Group (VG-20-03, outcrop); signals at the elution position of triaromatic ergosteroids are too low for positive identification, but stigmasteroids are clearly beneath detection limits (see comment in c). g, The AGSO-II industrial standard for comparison of triaromatic steroid elution positions.

Extended Data Table 1 Information on Proterozoic samples
Full size table
Extended Data Table 2 Indigenous Tonian and Cryogenian sterane and triaromatic steroid data
Full size table

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Brocks, J., Jarrett, A., Sirantoine, E. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017). https://doi.org/10.1038/nature23457

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