The origin of the eukaryotic cell is one of the major evolutionary events in the history of life on our planet. However, the mosaicism of the eukaryotic genome is challenging. Bacteria, Archaea, and Eukarya share common ancestry but they have very distinctive features. The eukaryotic cell differs by its much simpler prokaryote relatives, by possessing not only a nucleus, but also a complex cytoskeleton, a sophisticated endomembrane system, and mitochondria, the last of these, the result of an ancient endosymbiosis with a proteobacterium. Recently, the discovery in deep marine sediment of the Asgard archaea, a group closely related to eukaryotes, could lead us to unravel the origin of eukaryotes.
The term ‘FECA’, the first eukaryotic common ancestor, is often used to refer to the initial lineage of total group eukaryotes, just after its split from its closest living relative. By contrast, ther term ‘LECA’, the last eukaryotic common ancestor, refers to the ancestor only of extant eukaryotes (all known ones) plus extinct post-LECA lineages. Eukaryogenesis is the interval between FECA and LECA, when the characters that define the crown group evolved. LECA is generally believed to have lived during the Mesoproterozoic era, about 1.6 to 1 billion years ago, or possibly somewhat earlier. The age of FECA is even more uncertain. Based on the earliest widely acceptable eukaryote fossils, FECA had arrived some time before 1.9 Ga. Some models suggest a younger age for LECA. Hence, Mesoproterozoic rocks dominantly preserve stem group eukaryotes.
To understand the paths from FECA to LECA, it is necessary to identify eukaryote characters correctly in the deep fossil record. Therefore, the key to reconstructing the origin of eukaryotes lies in the integration of modern cell biology, molecular phylogeny, and the fossil record.
So, how do we recognize ancient fossils as eukaryotic? Size is a relevant parameter. On average, eukaryotic cells are substantially larger than those of prokaryotes, with diameters ranging from 10 to 100 μm. Another feature widespread among all eukaryotic supergroups is the formation of resistant-walled structures known as cysts. These forms are recognized in the fossil record by the presence of openings, spines or complex ornamentation. Some prokaryotes can be large too, and they can have processes and preservable walls. But none of them present these three characters at the same time. By contrast, eukaryotes exhibit these features in combination. Shuiyousphaeridium, one of the oldest evidence of eukaryotes, is a large, spiny, ornamented, organic walled microfossil found in latest Paleoproterozoic rocks. This form is an extinct genus of acritarch discovered in 1993.
Acritarchs are a heterogeneous and polyphyletic group of organic-walled microfossils of unknown affinity, consisting of a central cavity enclosed by a wall of single or multiple layers, with a great variability of shapes and ornamentations. The wall is made by sporopollenine or a very similar compound and the size range is about 5 to 200 micrometers. The acritarchs were dominant forms of eukaryotic phytoplankton during the NeoProterozoic and the Paleozoic. These forms diversified markedly, in parallel with the Cambrian and Ordovician radiations of marine invertebrates.
The term was first introduced by Evitt in 1963 and means “undecided origin” (from the Greek akritos = undecided, and arche = origin”), and replaced the older group “hystricosphaerid”. Based on their morphology, acritarchs are divided in nine groups: sphaeromorph, acanthomorphs, polygonomorphs, netromorphs, diacromorphs, prismatomorphs, oomorphs, herkomorphs, and pteromorphs.
The iconic Grypania spiralis has been questioned as eukaryotic. This coiled ribbon-like impression, was ﬁrst discovered in the Greyson Shale and Chamberlain Shale of the Mesoproterozoic Ravalli Group, in Montana, western USA. An alternative interpretation suggest that Grypania was a giant cyanobacterium.
One of the oldest multicellular organisms is Bangiomorpha pubescens. This extraordinary fossil provides the earliest unambiguous record of photosynthetic eukaryotic life. The individual filaments of the fossil are up to 2 mm long, and are composed of a single series of cells, or of several series running side by side, or a combination of the two, as in modern Bangia. The age of its first appearance was ~ 1.047 Ga. Other early multicellular eukaryotes include Palaeastrum, and Proterocladus. Those much younger fossils appeared only 800 million years ago.
While some questions still remains unanswered, the continued studies of the fossil record and biomarker assemblages may allow us to identify the environmental conditions that allowed the appearance of complex life.
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