When a tree isn’t actually a tree.

Elton John may have first introduced the idea in his hit song, Circle of Life, but a similar phrase has found its way into science. Undoubtedly Elton John considered only charismatic megafauna in his song, but if applied to the three Kingdoms of life, a circular evolutionary model arises. It is my suspicion that the authors Rivera and Lake tossed around the term “Circle of Life” during the preparation of their manuscript, but wisely chose against The Lion King reference. The Ring of Life idea was first brought to light in 2004, but still appears in textbooks and is widely cited, thus it deserves some revisiting.

Figure 1: Since the time of Darwin, the Tree of Life has been used to represent the evolutionary relationships among species. However, a more accurate representation may be a Circle of Life (Elton John, The Lion King), a Web of Life (Bapteste & Walsh 2005), or a Ring of Life (Rivera & Lake 2004).

Lake and Rivera pioneered a novel new algorithm based on gene content, called conditoned reconstruction, for genome based tree construction. This approach relies on the analogy gene:genome as nucleotide:gene. During evolution the orthologous gene can become either present (P) or absent (A). Thus a genome alignment can occur and Markov models can be applied to reconstruct the evolutionary history. Because genome comparison across all domains of life is impossible,  Lake and Rivera introduce a ‘conditioning genome’ to serve as a reference to compare genomes. This type of analysis can detect the fusion of two genomes opposed to the several large lateral gene transfers.

Rivera and Lake applied this model to eight genomes (3 Bacteria, 3 Archea, and 2 Eukaryotes). The resulting 5 trees are shown in Figure 2. The cumulative probabilites of these trees is shown at the right. The unrooted trees are shifted so a repeating pattern is revealed which indicates that the trees are actually variations of an underlying cyclic pattern. The rings shown at the bottom of Figure 2 are the compilation of the 5 trees, and when cut at any of the 5 arcs and unraveled, the resulting tree is one of the original 5 trees.

Figure 2. The 5 most probable trees in order of decreasing bootstrap support. From top to bottom: 60.5%, 16.8%, 10%, 7.2%, and 1.8% support. Fully resolved ring is at left and partially resolved ring is on the right. Results are based on 2,408 orthologousgene sets. From Rivera and Lake (2004).

These results strongly support the conclusion that 2 prokaryotic genomes fused, resulting in the first eukaryote. Rivera and Lake conclude the eukaryotic nuclear genome formed from the fusion of a proteobacterium and an archael eocyte (see Fig 3). Because a fusion organism connects two nodes of a ring, the removal of the fusion organisms will open the ring and convert it into a tree. The ring opened only when the 2 eukaryotes (yeast) were removed which indicates that the yeast lineage is the product of prokaryotes. Rivera and Lake also add to the evidence that in the Eukaryotic genome, informational genes derived from Archea and operational genes from Bacteria during the two genome fusion event.

Figure 3. Ring of Life schematic. The Tree of Life is indeed more ring-like than trunk-like according to the analysis of Rivera and Lake. The eukaryote resulted from the fusion of an archaen (eocyta and euryarchae) and a bacteria (proteobacteria, cyanobacteria, and bacilli). From Rivera and Lake (2004).

If coroborated, this Ring of Life provides a signifiicant departure from a long accepted evolutionary theory. In a subsequent paper, Bapteste and Walsh  (2005) claim that Rivera and Lake misrepresent lateral (horizontal) gene transfer and provide criticm of the methods. Since 2005 the Ring of Life has fallen out of favor, but many scientists believe it may be true and it just needs adequate support. As Elton John sings, “In the Circle of Life/ There’s far to much to take in here/ More to find that can ever be found”. The Tree of Life has been ever evolving and much debated, but leave it up to scientists, the answer will be found.

Works Cited:

Lake, J.A. and Rivera, M.C. (2004) Deriving the genomic tree of life in the presence of horizontal gene transfer: conditioned reconstruction. Mol. Biol. Evol. 21, 681–690

Rivera, M.C. and Lake, J.A. (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155

Bapteste, E. and Walsh, D.A. (2005) Does the ‘Ring of Life’ ring true? Trends Microbiol, 13, 256-261

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