Molecular paleontology and complexity in the last eukaryotic common ancestor

Abstract

Eukaryogenesis, the origin of the eukaryotic cell, represents one of the fundamental evolutionary transitions in the history of life on earth. This event, which is estimated to have occurred over one billion years ago, remains rather poorly understood. While some well-validated examples of fossil microbial eukaryotes for this time frame have been described, these can provide only basic morphology and the molecular machinery present in these organisms has remained unknown. Complete and partial genomic information has begun to fill this gap, and is being used to trace proteins and cellular traits to their roots and to provide unprecedented levels of resolution of structures, metabolic pathways and capabilities of organisms at these earliest points within the eukaryotic lineage. This is essentially allowing a molecular paleontology. What has emerged from these studies is spectacular cellular complexity prior to expansion of the eukaryotic lineages. Multiple reconstructed cellular systems indicate a very sophisticated biology, which by implication arose following the initial eukaryogenesis event but prior to eukaryotic radiation and provides a challenge in terms of explaining how these early eukaryotes arose and in understanding how they lived. Here, we provide brief overviews of several cellular systems and the major emerging conclusions, together with predictions for subsequent directions in evolution leading to extant taxa. We also consider what these reconstructions suggest about the life styles and capabilities of these earliest eukaryotes and the period of evolution between the radiation of eukaryotes and the eukaryogenesis event itself.

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

“…The position of Metamonada, the third major lineage of Excavata, with respect to the root advocated by Derelle et al (138), remains to be established. An important aspect of the recent rooting hypotheses is that all predict that the LECA was a complex, fully fledged eukaryote (96,138,139). The Opimoda-Diphoda rooting further suggests that the LECA was a biflagellated bacteriovorous excavate-like organism (resembling malawimonads and jakobids?)…”

Eukaryotic Flagella: Variations in Form, Function, and Composition during Evolution

“…Using the wealth of information provided in annotated genome sequences, comparative analyses of protein-coding gene repertoires in taxa spanning the breadth of eukaryotic evolution indicate the hallmark characteristics of eukaryotic cell biology -a nucleus, endomembrane and vesicular trafficking systems, mitochondrial metabolism, a cytoskeleton based on actin and microtubules -were all surprisingly well advanced in the last common ancestor of extant eukaryotes (Koumandou et al 2013). This includes the presence of a flagellum or flagella in that last common ancestor.…”

Arfs at a Glance

“…The Arf GTPase activating proteins (GAPs) catalyze the hydrolysis of GTP on their substrate Arf through a conserved domain that contains a zinc finger (Cukierman et al, 1995). The last common ancestor of modern eukaryotic cells likely possessed only one Arf family member, in contrast to having nearly 20 Rab proteins (Koumandou et al, 2013). Multiple Arf GEFs and GAPs existed in this ancient eukaryote, supporting the idea that a key feature of Arf function is a single Arf protein participating in multiple GEF and GAP regulatory complexes (Koumandou et al, 2013;Schlacht et al, 2013).…”