Earth’s earliest non-marine eukaryotes

Abstract

The existence of a terrestrial Precambrian (more than 542 Myr ago) biota has been largely inferred from indirect chemical and geological evidence associated with palaeosols1,2, the weathering of clay minerals3 and microbially induced sedimentary structures in siliciclastic sediments4. Direct evidence of fossils within rocks of non-marine origin in the Precambrian is exceedingly rare5,6. The most widely cited example comprises a single report of morphologically simple mineralized tubes and spheres interpreted as cyanobacteria, obtained from 1,200-Myr-old palaeokarst in Arizona5. Organic-walled microfossils were first described from the non-marine Torridonian (1.2–1.0 Gyr ago) sequence of northwest Scotland in 19077. Subsequent studies8,9,10 found few distinctive taxa—a century later, the Torridonian microflora is still being characterized as primarily nondescript “leiospheres”11. We have comprehensively sampled grey shales and phosphatic nodules throughout the Torridonian sequence. Here we report the recovery of large populations of diverse organic-walled microfossils extracted by acid maceration, complemented by studies using thin sections of phosphatic nodules that yield exceptionally detailed three-dimensional preservation. These assemblages contain multicellular structures, complex-walled cysts, asymmetric organic structures, and dorsiventral, compressed organic thalli, some approaching one millimetre in diameter. They offer direct evidence of eukaryotes living in freshwater aquatic and subaerially exposed habitats during the Proterozoic era. The apparent dominance of eukaryotes in non-marine settings by 1 Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought.

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Figure 1: Sphaeromorph acritarchs and cell clusters from the Torridonian, NW Scotland.
Figure 2: Cell clusters and large, morphologically complex vesicles.
Figure 3: Non-vesicular organic structures.

References

  1. 1

    Ohmoto, H. Evidence in pre-2.2 Ga paleosols for the early evolution of atmospheric oxygen and terrestrial biota. Geology 24, 1135–1138 (1996)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Gutzmer, J. & Beukes, N. J. Earliest laterites and possible evidence for terrestrial vegetation in the Early Proterozoic. Geology 26, 263–266 (1998)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Kennedy, M., Droser, M., Mayer, L. M., Pevear, D. & Mrofka, D. Late Precambrian oxygenation; inception of the clay mineral factory. Science 311, 1446–1449 (2006)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Prave, A. R. Life on land in the Proterozoic: evidence from the Torridonian rocks of northwest Scotland. Geology 30, 811–814 (2002)

    ADS  Article  Google Scholar 

  5. 5

    Horodyski, R. J. & Knauth, L. P. Life on land in the Precambrian. Science 263, 494–498 (1994)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Schopf, J. W. & Klein, C. The Proterozoic Biosphere (Cambridge Univ. Press, 1992)

    Google Scholar 

  7. 7

    Teall, J. J. H. in The Geological Structure of the North-west Highlands of Scotland (eds Peach, B. N. et al.) 288, plate LII (Memoirs of the Geological Society of Great Britain, 1907)

    Google Scholar 

  8. 8

    Downie, C. So-called spores from the Torridonian. Proc. Geol. Soc. Lond. 1600, 127–128 (1962)

    Google Scholar 

  9. 9

    Cloud, P. E. & Germs, A. New pre-Paleozoic nannofossils from the Stoer Formation (Torridonian), NW Scotland. Geol. Soc. Am. Bull. 82, 3469–3474 (1971)

    ADS  Article  Google Scholar 

  10. 10

    Zhang, Z. Upper Proterozoic microfossils from the Summer Isles, N.W. Scotland. Palaeontology 25, 443–460 (1982)

    Google Scholar 

  11. 11

    Kinnaird, T. C. et al. The late Mesoproterozoic-early Neoproterozoic tectonostratigraphic evolution of NW Scotland: the Torridonian revisited. J. Geol. Soc. Lond. 164, 541–551 (2007)

    Article  Google Scholar 

  12. 12

    Turnbull, M. J. M., Whitehouse, M. J. & Moorbath, S. New isotopic age determinations for the Torridonian, NW Scotland. J. Geol. Soc. Lond. 153, 955–964 (1996)

    CAS  Article  Google Scholar 

  13. 13

    Parnell, J., Boyce, A. J., Mark, D., Bowden, S. & Spinks, S. Early oxygenation of the terrestrial environment during the Mesoproterozoic. Nature 468, 290–293 (2010)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Stewart, A. D. The Later Proterozoic Torridonian Rocks of Scotland: Their Sedimentology, Geochemistry and Origin (Memoirs of the Geological Society, no. 24, 2002)

    Google Scholar 

  15. 15

    Stewart, A. D. Greywacke sedimentation in the Torridonian of Colonsay and Oronsay. Geol. Mag. 99, 399–419 (1962)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Sutton, J. & Watson, J. Sedimentary structures in the epidotic grits of Skye. Geol. Mag. 97, 106–122 (1960)

    ADS  Article  Google Scholar 

  17. 17

    Stewart, A. D. & Parker, A. Palaeosalinity and environmental interpretation of red beds from the late Precambrian (‘Torridonian’) of Scotland. Sedim. Geol. 22, 229–241 (1979)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Phil. Trans. R. Soc. B 361, 1023–1038 (2006)

    CAS  Article  Google Scholar 

  19. 19

    Meng, F., Zhou, C., Yin, L., Chen, Z. & Yuan, X. The oldest known dinoflagellates: morphological and molecular evidence from Mesoproterozoic rocks at Yongji, Shanxi Province. Chin. Sci. Bull. 50, 1230–1234 (2005)

    Article  Google Scholar 

  20. 20

    Jankauskas, T. V., Mikhailova, N. S. & Hermann, T. N. in Mikrofossilii Dokembriya SSSR [Precambrian Microfossils of the USSR] 190 (Nauka, Leningrad, 1989)

    Google Scholar 

  21. 21

    Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66–69 (2001)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Knoll, A. H. Microbiotas of the late Precambrian Hunnberg Formation, Nordaustlandet, Svalbard. J. Paleontol. 58, 131–162 (1984)

    Google Scholar 

  23. 23

    Butterfield, N. J. & Chandler, F. W. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35, 943–957 (1992)

    Google Scholar 

  24. 24

    Mikhailov, K. V. et al. The origin of Metazoa: a transition from temporal to spatial cell differentiation. Bioessays 31, 758–768 (2009)

    CAS  Article  Google Scholar 

  25. 25

    Butterfield, N. J. Modes of pre-Ediacaran multicellularity. Precambr. Res. 173, 201–211 (2009)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Blank, C. E. & Sánchez-Baracalo, P. Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise in atmospheric oxygen. Geobiology 8, 1–23 (2010)

    CAS  Article  Google Scholar 

  27. 27

    Lenton, T. M. & Watson, A. J. Biotic enhancement of weathering, atmospheric oxygen and carbon dioxide in the Neoproterozoic. Geophys. Res. Lett. 31, 1–5 (2004)

    Article  Google Scholar 

  28. 28

    Knauth, L. P. & Kennedy, M. J. The late Precambrian greening of the Earth. Nature 460, 728–732 (2009)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Spinks, S. C., Parnell, J. & Bowden, S. A. Reduction spots in the Mesoproterozoic age: implications for life in the early terrestrial record. Int. J. Astrobiol. 9, 209–216 (2010)

    CAS  Article  Google Scholar 

  30. 30

    Hutchinson, G. E. The paradox of the plankton. Am. Nat. 95, 137–145 (1961)

    Article  Google Scholar 

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Acknowledgements

J. Rosenberg produced the confocal laser scanning image (Supplementary Fig. 6a); we thank O. Green for preparation of phosphatic nodules at Oxford. We thank J. Antcliffe, R. Callow and S. Moorhouse for field assistance and the people of Scoraig and Bill (the boatman) for access to Cailleach Head. This research was supported by NASA grant NNX07AU79G (P.K.S.), NERC NE/G015716/1 (C.H.W.) and NERC NE/G524060/1 (L.B.).

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All authors contributed to the intellectual content, design and writing of the manuscript, and collection and study of phosphatic nodules. C.H.W. and P.K.S. collected the palynological samples. P.K.S. wrote an initial draft, prepared the photographic plates and produced the provisional taxonomic assessment. L.B. and C.H.W. drafted the figures.

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Correspondence to Paul K. Strother.

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The authors declare no competing financial interests.

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All materials (rock sample, remaining organic residues, palynological slides, thin sections) are curated in the collections of the Centre for Palynology of the University of Sheffield, UK.

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This file contains Supplementary Figures 1-7 with legends and Supplementary Tables 1-2. (PDF 5122 kb)

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Strother, P., Battison, L., Brasier, M. et al. Earth’s earliest non-marine eukaryotes. Nature 473, 505–509 (2011). https://doi.org/10.1038/nature09943

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