Gene similarity networks provide tools for understanding eukaryote origins and evolution

Abstract

The complexity and depth of the relationships between the three domains of life challenge the reliability of phylogenetic methods, encouraging the use of alternative analytical tools. We reconstructed a gene similarity network comprising the proteomes of 14 eukaryotes, 104 prokaryotes, 2,389 viruses and 1,044 plasmids. This network contains multiple signatures of the chimerical origin of Eukaryotes as a fusion of an archaebacterium and a eubacterium that could not have been observed using phylogenetic trees. A number of connected components (gene sets with stronger similarities than expected by chance) contain pairs of eukaryotic sequences exhibiting no direct detectable similarity. Instead, many eukaryotic sequences were indirectly connected through a "eukaryote-archaebacterium-eubacterium-eukaryote" similarity path. Furthermore, eukaryotic genes highly connected to prokaryotic genes from one domain tend not to be connected to genes from the other prokaryotic domain. Genes of archaebacterial and eubacterial ancestry tend to perform different functions and to act at different subcellular compartments, but in such an intertwined way that suggests an early rather than late integration of both gene repertoires. The archaebacterial repertoire has a similar size in all eukaryotic genomes whereas the number of eubacteriumderived genes is much more variable, suggesting a higher plasticity of this gene repertoire. Consequently, highly reduced eukaryotic genomes contain more genes of archaebacterial than eubacterial affinity. Connected components with prokaryotic and eukaryotic genes tend to include viral and plasmid genes, compatible with a role of gene mobility in the origin of Eukaryotes. Our analyses highlight the power of network approaches to study deep evolutionary events.mobile genetic elements | cellular evolution | network analysis | organelles | recombination

Horizontal gene flow from Eubacteria to Archaebacteria and what it means for our understanding of eukaryogenesis

“…Tha, Thaumarchaeota; Nan, Nanoarchaeota; Sul, Sulfolobales; Thc, Thermococcales; Thr, Thermoproteales; Des, Desulfurococcales; Aci, Acidolobales; Acu, through processes of endosymbiosis, whereby the symbiont was progressively simplified and its genes transferred to the host nucleus. Similar simplification processes are known to have happened in eukaryotic organelles [74], nucleomorphs [7], and in extant animal symbionts like the Blochmannia floridanus symbionts of ants [75]. Nelson-Sathi et al [37] identified six archaebacterial groups the origins of which seem to have been coincident with largescale imports from Eubacteria.…”

The ring of life hypothesis for eukaryote origins is supported by multiple kinds of data

“…This allows a test of the association between evolutionary history and function. When eukaryotic genes with prokaryote homologues are partitioned into one class that are homologous with archaebacterial genes and another class that are homologous to eubacterial genes, we see that the genes that are homologous to Archaebacteria are more likely to be lethal upon deletion, they are more highly expressed than the eubacterial genes, the protein products are significantly more central in protein interaction networks (PINs) and are usually under more selective constraint (as judged by dN/dS ratios) [82,83,85]. In addition, there is an interesting difference between eukaryotic genes with archaebacterial homologues and those with eubacterial homologues-the eubacterial homologues are more likely to be duplicated in large eukaryotic genomes and are more likely to be lost in small eukaryotic genomes.…”

“…Analyses of homologies between eukaryotes and prokaryotes have consistently found a disjoint between the relationships that have been inferred [69,[82][83][84][85] (see supporting information, figure S3, for Alvarez-Ponce et al [85]-http:// archaebacterial.pnas.org/content/suppl/2013/04/01/121137 1110.DCSupplemental/sapp.pdf). In general, while there are many gene families that are found across all three groups, quite often we find gene families that are found in only two of the three groups (i.e.…”

Evolution by Pervasive Gene Fusion in Antibiotic Resistance and Antibiotic Synthesizing Genes

“…Networks were traditionally used in non-scientific fields, for example, in the mapping of railroads [7] and more recently in friendship relationships on social network sites such as Facebook [8]. Recently, this approach has been adapted to better understand evolution [1,[9][10][11][12]. Through the use of SSNs, Halary et al [13] investigated a molecular dataset of 571,044 protein sequences from the three domains of life.…”

“…SSNs are generally composed of one or more connected components (CCs). A CC consists of directly or indirectly related sequences, without the need for all sequences to display detectable homology to one another [12]. Genes identified as part of a clique, are usually, though not necessarily, functionally similar [16].…”