Research ArticlePALEONTOLOGY

Experimental taphonomy of organelles and the fossil record of early eukaryote evolution

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Science Advances  27 Jan 2021:
Vol. 7, no. 5, eabe9487
DOI: 10.1126/sciadv.abe9487
  • Fig. 1 Percentage of algal cells that have characteristics of decay.

    Acquisition of different features as decay progresses in oxic and anoxic groups. Samples were taken while the algae were alive (L), immediately after death (FK), and every 2 to 3 days for 6 weeks. The development of holes in Rhodochorton was particularly noticeable, and so this was measured separate from the collapse of the chloroplast edges. In P. morum, the cells themselves collapsed after death.

  • Fig. 2 Decay of V. aureus and P. morum.

    (A to F) V. aureus and (G to L) P. morum. Living colonies of V. aureus (A) show clear cell boundaries and structure, but after death, the colonies display some disaggregation (B). As decay progresses, chloroplasts become less regular in shape (C and E) and develop holes and thin patches (F). Pyrenoids disappear from within the chloroplast, leaving holes ringed by starch grains with no pyrenoid visible (D and E). Some nuclei were still visible weeks after death with no evidence of deformation (C and E). Living colonies of P. morum are closely arranged (G), but this collapses after cell death, resulting in the loss of Y-shaped junctions (H). One chloroplast was observed leaving the cell in a cloud (I), but usually, chloroplasts developed holes and thin patches as they decayed (J and K). In late stages of decay, small amounts of green chloroplast were left surrounding the remnants of the starch grain ring (L). Nuclei could still be observed well into decay (K and L). Pyrenoids decayed quickly to leave empty starch grain rings, but this varied within colonies, with some cells still with visible pyrenoids (J and L). n, nucleus; c, chloroplast; s, starch grain ring; p, pyrenoid; y, Y-shaped junction; t/h, thinning/holes within the chloroplast. The number of days postmortem is indicated in the top right corner. Scale bars, 50 μm (A), 91.4 μm (B), 9.1 μm (C), 9.0 μm (D), 9.0 μm (E), 9.1 μm (F), 7.8 μm (G), 6.3 μm (H), 9.1 μm (I), 9.1 μm (J), 9.1 μm (K), and 9.0 μm (L).

  • Fig. 3 Decay of Chlorella sp. and Rhodochorton sp.

    (A to G) Chlorella sp. and (H to N) Rhodochorton sp. Living cells of Chlorella (A) show little difference from those immediately after death (B). As decay progresses, chloroplasts collapse, becoming less regular in shape (C and D). Pyrenoids disappear quickly, leaving empty starch grain rings (E), while chloroplasts thin and develop holes (D to F). Nuclei could still be observed in some cells (C, F, and G). In some cases, the chloroplast can escape the cell (F). Living Rhodochorton cells (H) also show little difference from those immediately after death, although chloroplasts collapse and deform quickly (I). Holes develop within the chloroplasts (J and K) and in later stages of decay can occasionally conglomerate along the cell walls along with the cytoplasmic contents (L) or pull away from the cell wall (M). Nuclei can still be observed in some cells, even when much of the cytoplasm is gone (K and N). The number of days postmortem is indicated in the top right corner. Scale bars, 10 μm (A), 18.7 μm (B), 15 μm (C), 18.5 μm (D), 18.4 μm (E), 15.8 μm (F), 18.7 μm (G), 12.6 μm (H), 11.8 μm (I), 14.9 μm (J), 15.4 μm (K), 14.1 μm (L), 10.4 μm (M), and 14.8 μm (N).

  • Fig. 4 Fossil organelles.

    (A) Fossil of a Zelkova leaf from the Miocene Succor Creek Formation showing a chloroplast adpressed to the cell wall, with grana stacks visible and a densely stained starch grain. Transmission electron micrograph after a carbohydrate cytochemical analysis; image from (29) courtesy of Karl Niklas, Cornell University. (B) Segment of the stem of a royal fern from Jurassic deposits with clear nuclei in each cell. Light micrograph; image courtesy of Benjamin Bomfleur, University of Münster. (C) Tomographic virtual section through Megasphaera, a fossil from the Weng’an Biota that is suggested to have nuclei. Data courtesy of (35). (D) Intracellular structures in the holotype of R. chitrakootensis have previously been interpreted as pyrenoids but are unlikely to be so. Tomographic reconstruction; data from (41) courtesy of Stefan Bengtson, Swedish Museum of Natural History. (E) Bangiomorpha pubescens, currently considered the oldest crown eukaryote. Light micrograph; image courtesy of Nicholas Butterfield, University of Cambridge. (F) Caryosphaeroides and (G) Glenobotrydion from the Bitter Springs Biota have been suggested to be early eukaryotes with putative nuclei or chloroplasts. Light micrographs; images from (38) courtesy of SEPM. (H) Shuiyousphaeridium and (I) Dictyosphaera from the Ruyang Group, putative early eukaryotes with intracellular structures suggested to be nuclei or collapsed cellular contents. Light micrographs; images courtesy of Shuhai Xiao, Virginia Tech. (J) Leptoteichos from the Gunflint Iron Formation with a putative nucleus. Light micrograph; image from (45) courtesy of SEPM (Society for Sedimentary Geology) (SEPM). Scale bars, 1.4 μm (A), 25.6 μm (B), 250 μm (C), 38.2 μm (D), 25 μm (E), 3.3 μm (F), 13.8 μm (G), 14.3 μm (H), 25.3 μm (I), and 3.5 μm (J).

Supplementary Materials

  • Supplementary Materials

    Experimental taphonomy of organelles and the fossil record of early eukaryote evolution

    Emily M. Carlisle, Melina Jobbins, Vanisa Pankhania, John A. Cunningham, Philip C. J. Donoghue

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