Koonin: The Origin and Early Evolution of Eukaryotes in the Light of Phylogenomics
Readers will find this review paper by Eugene Koonin useful. It was published in 2010.
The origin of eukaryotes is a huge enigma and a major challenge for evolutionary biology [1-3]. There is a sharp divide in the organizational complexity of the cell between eukaryotes, which have complex intracellular compartmentalization, and even the most sophisticated prokaryotes (archaea and bacteria), which do not [4-6]. A typical eukaryotic cell is about 1,000-fold bigger by volume than a typical bacterium or archaeon, and functions under different physical principles: free diffusion has little role in eukaryotic cells, but is crucial in prokaryotes [7,8]. The compartmentalization of eukaryotic cells is supported by an elaborate endomembrane system and by the actin-tubulin-based cytoskeleton [9,10]. There are no direct counterparts of these organelles in archaea or bacteria. The other hallmark of the eukaryotic cell is the presence of mitochondria, which have a central role in energy transformation and perform many additional roles in eukaryotic cells, such as in signaling and cell death.
The conservation of the major features of cellular organization and the existence of a large set of genes that are conserved across eukaryotes leave no doubt that all extant eukaryotic forms evolved from a last eukaryote common ancestor (LECA; see below). All eukaryotes that have been studied in sufficient detail possess either mitochondria or organelles derived from mitochondria [11-13], so it is thought that LECA already possessed mitochondria (see below). Plants and many unicellular eukaryotes also have another type of organelle, plastids.
The organizational complexity of the eukaryotic cells is complemented by extremely sophisticated, cross-talking signaling networks [14]. The main signaling systems in eukaryotes are the kinase-phosphatase machinery that regulates protein function through phosphorylation and dephosphorylation [15-18]; the ubiquitin network that governs protein turnover and localization through reversible protein ubiquitylation [19-21]; regulation of translation by microRNAs [22-24]; and regulation of transcription at the levels of individual genes and chromatin remodeling [24-27]. Eukaryotes all share the main features of cellular architecture and the regulatory circuitry that clearly differentiate them from prokaryotes, although the ancestral forms of some signature eukaryotic systems are increasingly detected in prokaryotes, as discussed below. Phylogenomic reconstructions show that the characteristic eukaryotic complexity arose almost ‘ready made’, without any intermediate grades seen between the prokaryotic and eukaryotic levels of organization [9,28-30]. Explaining this apparent leap in complexity at the origin of eukaryotes is one of the principal challenges of evolutionary biology.
The key to the origin of eukaryotes will undoubtedly be found using comparative genomics of eukaryotes, archaea and bacteria. Complete genome sequences from all three domains of cellular life are accumulating exponentially, albeit at markedly different paces. As of March 2010, the NCBI genome database contained over 1,000 bacterial genomes, about 100 archaeal genomes, and about 100 genomes of eukaryotes [31]. Here, I discuss some of the main insights that have come from comparative analysis of these genomes, which may help to shed light on the origin and the early stages of evolution of eukaryotes. So far, the comparative genomics era has brought fascinating clues but no decisive breakthrough.
