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. 2009 May 25:1:99-113.
doi: 10.1093/gbe/evp011.

Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes

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Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes

Igor B Rogozin et al. Genome Biol Evol. .

Abstract

The deep phylogeny of eukaryotes is an important but extremely difficult problem of evolutionary biology. Five eukaryotic supergroups are relatively well established but the relationship between these supergroups remains elusive, and their divergence seems to best fit a "Big Bang" model. Attempts were made to root the tree of eukaryotes by using potential derived shared characters such as unique fusions of conserved genes. One popular model of eukaryotic evolution that emerged from this type of analysis is the unikont-bikont phylogeny: The unikont branch consists of Metazoa, Choanozoa, Fungi, and Amoebozoa, whereas bikonts include the rest of eukaryotes, namely, Plantae (green plants, Chlorophyta, and Rhodophyta), Chromalveolata, excavates, and Rhizaria. We reexamine the relationships between the eukaryotic supergroups using a genome-wide analysis of rare genomic changes (RGCs) associated with multiple, conserved amino acids (RGC_CAMs and RGC_CAs), to resolve trifurcations of major eukaryotic lineages. The results do not support the basal position of Chromalveolata with respect to Plantae and unikonts or the monophyly of the bikont group and appear to be best compatible with the monophyly of unikonts and Chromalveolata. Chromalveolata show a distinct, additional signal of affinity with Plantae, conceivably, owing to genes transferred from the secondary, red algal symbiont. Excavates are derived forms, with extremely long branches that complicate phylogenetic inference; nevertheless, the RGC analysis suggests that they are significantly more likely to cluster with the unikont-Chromalveolata assemblage than with the Plantae. Thus, the first split in eukaryotic evolution might lie between photosynthetic and nonphotosynthetic forms and so could have been triggered by the endosymbiosis between an ancestral unicellular eukaryote and a cyanobacterium that gave rise to the chloroplast.

Keywords: deletions; eukaryotic phylogeny; insertions; parsimony; rare genomic changes; substitutions.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
Competing topologies of the evolutionary tree of eukaryotes. (A) Crown-group topology (B) The Big Bang radiation of the five supergroups (C) The unikont–bikont topology. The trees are rendered in a simplified form, with only well-characterized groups for which complete genome sequences are available and that were included in the present analysis denoted explicitly. The branch lengths are arbitrary.
F<sc>IG</sc>. 2.—
FIG. 2.—
Examples of the RGCs used in this work (A) RGC_CAM: KOG0370 (B) RGC_CA: KOG0370 (C) RGC_DELL: KOG0435 (D) RGC_INS: KOG2509. For RGC_CAM (A) and RGC_CA (B), the corresponding codons extracted from the underlying nucleotide sequence alignments are shown in parentheses. The RGC positions are shown in green (five prokaryotic species used as the outgroup), red (plants), and blue (fungi, animals). H. sapiens (Hs), A. gambiae (Ag), C. elegans (Ce), D. melanogaster (Dm), S. cerevisiae (Sc), S. pombe (Sp), A. thaliana (At), O. sativa (Os), and five outgroup prokaryotic species (P1P5).
F<sc>IG</sc>. 3.—
FIG. 3.—
The analyzed trifurcations of major eukaryotic lineages. For each analyzed trifurcation, the lengths of branches in the number of RGC_CAMs are indicated. Balanced trifurcation indicates that all three analyzed branches are of approximately equal lengths (the lengths are not significantly different as suggested by the χ2 test with 2 degrees of freedom); otherwise, that is, when there is a statistically significant difference in branch lengths, a trifurcation is considered to be unbalanced.
F<sc>IG</sc>. 4.—
FIG. 4.—
The scenario of evolution of eukaryotic supergroups that is best compatible with the results of the RGC analysis. The primary (postmitochondrial) endosymbiosis of a cyanobacterium with an ancient, heterotrophic, unicellular eukaryote that is thought to have precipitated the first split in the evolution of eukaryotes, that between photosynthesis and nonphotosynthetic organisms, and the secondary endosymbiosis of a red alga and a nonphotosynthetic unicellular form, which would trigger the divergence of chromalveolates from the unikont lineage, are schematically shown. The oval shape encases the traditional unikont supergroup. The excavates are shown as a single branch, although their monophyly remains uncertain as well as their position in the tree; to emphasize this uncertainty, the excavate branch is shown with a dashed line. The branch lengths are arbitrary.

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