Nucleus preservation in early Ediacaran Weng'an embryo-like fossils, experimental taphonomy of nuclei and implications for reading the eukaryote fossil record.

Weichen Sun,Maoyan Zhu,Zongjun Yin,Philip C J Donoghue,John A Cunningham,Pengju Liu

doi:10.1098/rsfs.2020.0015

Abstract

The challenge of identifying fossilized organelles has long hampered attempts to interpret the fossil record of early eukaryote evolution. We explore this challenge through experimental taphonomy of nuclei in a living eukaryote and microscale physical and chemical characterization of putative nuclei in embryo-like fossils from the early Ediacaran Weng'an Biota. The fossil nuclei exhibit diverse preservational modes that differ in shape, presence or absence of an inner body and the chemistry of the associated mineralization. The nuclei are not directly fossilized; rather, they manifest as external moulds. Experimental taphonomy of epidermal cells from the common onion (Allium cepa) demonstrates that nuclei are more decay resistant than their host cells, generally maintaining their physical dimensions for weeks to months post-mortem, though under some experimental conditions they exhibit shrinkage and/or become shrouded in microbial biofilms. The fossil and experimental evidence may be rationalized in a single taphonomic pathway of selective mineralization of the cell cytoplasm, preserving an external mould of the nucleus that is itself resistant to both decay and mineral replication. Combined, our results provide both a secure identification of the Weng'an nuclei as well as the potential of a fossil record of organelles that might help arbitrate in long-standing debates over the relative and absolute timing of the evolutionary assembly of eukaryote-grade cells.

Highlights

Interpreting the fossil record of eukaryotes is challenging because their key distinguishing characteristics—organelles and a nucleus—are not commonly preserved
We have shown that the controversial nucleus-like structures in the early Ediacaran Weng’an embryo-like fossils exhibit a diversity of preservational modes that differ in terms of their consistency of shape, presence or absence of an inner body and the nature of their mineralization
These structures are not preserved directly; rather, they manifest as external moulds in the mineralization of the remaining cell volume

Summary

Introduction

Interpreting the fossil record of eukaryotes is challenging because their key distinguishing characteristics—organelles and a nucleus—are not commonly preserved. This stems from experiments which show that cytoplasmic shrinkage in decaying bacteria can produce nucleus-like remains [2,3,4] It does not follow from these experiments that nuclei cannot be preserved and, there are a number of credible claims of fossilized nuclei [5,6,7,8,9,10,11,12,13,14]. Claims of nuclei and even nucleoli preserved in association with embryo-like fossils from the approximately 609 Mya Ediacaran Weng’an Biota [15,16,17,18,19,20] have proven especially contentious [1,21,22,23] These structures exhibit a consistent size and shape and generally occur one per cell except where two occur, bilaterally arranged, interpreted to anticipate the plane of cell division [16]. The style of fossilization that these structures exhibit and the fossilization potential of nuclei remain unclear

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