Earth’s earliest non-marine eukaryotes

Journal name:
Nature
Volume:
473,
Pages:
505–509
Date published:
DOI:
doi:10.1038/nature09943
Received
Accepted
Published online

The existence of a terrestrial Precambrian (more than 542Myr 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 (1.2–1.0Gyr 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 1Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought.

At a glance

Figures

  1. Sphaeromorph acritarchs and cell clusters from the Torridonian, NW Scotland.
    Figure 1: Sphaeromorph acritarchs and cell clusters from the Torridonian, NW Scotland.

    a, Leiosphaeridia crassa; TOR08-18/Glame Member, Applecross Formation. b, Acritarch similar to Trematoligotriletum emarginatum Tim. with irregular verrucate surface; TOR08-26/Allt na Beistre Member, Applecross Formation. c, Lophosphaeridium sp. enclosed in a thin membranous vesicle; TOR08-34/Diabaig Formation. d, Surface detail of inner cyst (Lophosphaeridium sp.) in c showing small, evenly distributed granae. e, Leiosphaeridia crassa exhibiting a median split; TOR08-45/Cailleach Head Formation. f, Ellipsoidal cyst with granular wall structure exhibiting a terminal circular pylome excystment feature (arrow); TOR08-34/Diabaig Formation. g, Coarsely corrugate vesicle with dense contents; TOR08-27/Diabaig Formation. h, Spherical ball of cells enclosed within a complex wall (thin section from phosphatic nodule, Diabaig Formation). i, Blunt ellipsoidal vesicle with a micro-reticulate wall; TOR08-46/Cailleach Head Formation. j, Detail of i (box), showing the reticulate wall texture. k, Cell cluster, similar to Synsphaeridium sp. Note included condensed organic ‘spots’ (arrows); TOR08-26/Allt na Beistre Member, Applecross Formation. Scale bars: 10µm (ac, ei, k), 1µm (d, j).

  2. Cell clusters and large, morphologically complex vesicles.
    Figure 2: Cell clusters and large, morphologically complex vesicles.

    Lines in b and d demarcate edges of separate images used to construct the photo mosaics. a, Cell cluster exhibiting mutually adpressed cells with included ‘spots’ (arrowed). This image is a photomontage of three different focal planes (thin section from phosphatic nodule, Diabaig Formation). b, Large fusiform vesicle with pitted/reticulate wall structure; TOR08-9b/Kinloch Formation. c, Detail from b, showing a portion of the inside of the vesicle wall. d, Large vesicle with a dense central body (cb) and an asymmetric structure (as); TOR08-34/Diabaig Formation. e, Detail of the asymmetric structure in d. f, Transmitted infrared (>830nm) image of the central body in c, showing it to be a thick-walled, probably unicellular cyst. g, Large vesicle with a single-layered inner cyst and a large asymmetric structure (as) which appear as stubby projections from the main vesicle wall; TOR08-12/Kinloch Formation. Scale bars: 10µm (a, c, e, f); 50µm (b); 25µm (d, g).

  3. Non-vesicular organic structures.
    Figure 3: Non-vesicular organic structures.

    a, Oval plate with two blunt-tipped arms (arm), one of which is attached (ba, arrowed) with what appears to be a basal plug; TOR08-32/Diabaig Formation. b, Tri-lobed thalloid organism with a dense upper surface showing small cracks and a heterogeneous inner layer. Image is a photomontage of four photographs; TOR08-40/Diabaig Formation. c, Detail of b photographed in infrared (>830nm) transmitted light to reveal the internal structure. d, Spine (appendage?) tip; TOR08-34/Diabaig Formation. Scale bars: 50µm (a); 100µm (b); 10µm (c, d).

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Author information

Affiliations

  1. Department of Earth and Environmental Sciences, Boston College, Weston, Massachusetts 02493, USA

    • Paul K. Strother
  2. Department of Earth Sciences, University of Oxford, Parks Road, Oxford OX1 3PR, UK

    • Leila Battison &
    • Martin D. Brasier
  3. Department of Animal & Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK

    • Charles H. Wellman

Contributions

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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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  1. Supplementary Information (5M)

    This file contains Supplementary Figures 1-7 with legends and Supplementary Tables 1-2.

Comments

  1. Report this comment #19832

    Brig Klyce said:

    We commend Strother et al. for a careful study. But we cannot ignore a disparity between the treatment of their images and the microfossils seen by Richard B. Hoover and published in March. The former are easily accepted as biological, yet the latter are not! We invite your readers to compare the images.

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