The slow road to the eukaryotic genome

Abstract

The eukaryotic genome is a mosaic of eubacterial and archaeal genes in addition to those unique to itself. The mosaic may have arisen as the result of two prokaryotes merging their genomes, or from genes acquired from an endosymbiont of eubacterial origin. A third possibility is that the eukaryotic genome arose from successive events of lateral gene transfer over long periods of time. This theory does not exclude the endosymbiont, but questions whether it is necessary to explain the peculiar set of eukaryotic genes. We use phylogenetic studies and reconstructions of ancestral first appearances of genes on the prokaryotic phylogeny to assess evidence for the lateral gene transfer scenario. We find that phylogenies advanced to support fusion can also arise from a succession of lateral gene transfer events. Our reconstructions of ancestral first appearances of genes reveal that the various genes that make up the eukaryotic mosaic arose at different times and in diverse lineages on the prokaryotic tree, and were not available in a single lineage. Successive events of lateral gene transfer can explain the unusual mosaic structure of the eukaryotic genome, with its content linked to the immediate adaptive value of the genes its acquired. Progress in understanding eukaryotes may come from identifying ancestral features such as the eukaryotic splicesome that could explain why this lineage invaded, or created, the eukaryotic niche.

Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world

“…These architectures are associated with proteins that play diverse and fundamental functional roles in the cell, such as translational and transcriptional machinery, metabolic and signaling pathways, structural scaffolds, and many other aspects important for cellular function and interaction. The proteins themselves cannot capture adequately deep phylogenetic relationships because of the erasing effects of mutation and HGT; a comparative genomic exercise therefore reveals genomes as evolutionary mosaics of genes (Lester et al 2005). A focus on molecular designs that are immutable for extended periods of time rather than a focus on the vagaries of gene sequence uncovers here deep historical signatures.…”

“…The minimalist trend suggests an early split of life into two organismal groups, an archaeal-like ancestor undergoing proteome reduction and a eukaryal-like ancestor that retained the molecular complexity of the rich communal world. This caused modern Eukarya to be more closely related to Bacteria at gene sequence, gene content (e.g., Esser et al 2004;Lester et al 2005), and structural levels (e.g., Wang and CaetanoAnollés 2006), despite preserving many commonalities of the ancient protein world with Archaea, such as the phylogenetically ancestral components of the translation and transcription apparatus (Walsh and Doolittle 2005 Reductive tendencies were also present in the eukaryal-like ancestor, but involved fewer and younger architectures compared to Archaea. The first superkingdom-specific architecture appeared in Bacteria, signaling the "official" start of the superkingdom specification epoch.…”

The Pleasures and Perils of Darwinizing Culture (with Phylogenies)

“…This analysis grouped the birds by habitat, which suggested that convergent evolution driven by foraging mode had shaped these characters. More recently, Lester et al (2005) have used phylogenetic methods to study the evolution of the eukaryotic genome. By inferring the date that specific genes first appeared in prokaryote phylogenies, they were able to test the hypothesis that the eukaryote genome arose from successive horizontal transfer events.…”

Origin of eukaryotes as a symbiosis of parasitic α-proteobacteria in the periplasm of two-membrane-bounded sexual prekaryotes

“…In fact, their 'ring of life' can be an artifact of their analysis that can be easily substituted and reinterpreted by means of prokaryote-to-eukaryote serial horizontal gene transfer. 39,40 Metabolic symbiosis of an α-proteobacterium in an archeon. Martin and Müller 41 propose that eukaryotic cells arose as a symbiosis of hydrogen-producing α-proteobacteria in methanogenic hydrogen-consuming archaea (Hydrogen hypothesis).…”