THE ORIGIN OF INTRACELLULAR STRUCTURES IN EDIACARAN METAZOAN EMBRYOS

Animal embryo-like fossils from the Ediacaran Doushantuo Formation (635–551 Ma), South China, have been interpreted as the earliest metazoan fossils, geologically far prior to the radiation of biomineralizing animals and macroscopic bilaterians during the Ediacaran-Cambrian transition. While a recent reinterpretation of these fossils as giant sulfur-oxidizing bacteria may have called their metazoan affinity into question, the exceptional cellular and intracellular preservation of the Doushantuo fossils can provide tantalizing glimpses into the organellic structures of these potential multicellular eukaryotes. The organelle-like features are distinguishable in light, electron, and x-ray imaging, a distinction that has been assumed to be a result of compositional variation. This assumption has yet been verified, however. Using a combination of analytical techniques, including light microscopy, microcomputed x-ray tomography, scanning electron microscopy (SEM) secondary and backscatter (in both composition and topography modes) imaging, SEM-based energy dispersive x-ray spectroscopy, atomic force microscopy, and electron probe microanalyzer-based elemental spectroscopy, our results reveal, rather than compositional variation, that the visibility of these intracellular structures originates from crystalline textural variation. Specifically, the cell lumen and lipid vesicle-like (or yolk granule-like) structures are preserved as nm-sized randomly oriented apatite crystals, whereas cell boundaries and nucleus-like structures are preserved as botryoidal aggregates of μm-size apatite crystals. These textural differences indicate a two-stage taphonomic mineralization, and the botryoidal aggregates at the cell boundaries and nucleus-like structures represent late-stage overgrowth or void-filling cementation. Our findings therefore suggest that, while they may occupy the same topological position as strongly degraded nuclei and vesicles, the Doushantuo intracellular structures do not represent organelles with intact enclosing membranes. Instead, the membrane-like structures that characterize cell boundaries and nucleus-like structures are mostly late-stage cements that illustrate the essential role of degradation and mineralization in fossil preservation.