Abstract
Reconstructing the evolutionary history of modern species is a difficult problem complicated by the conceptual and technical limitations of phylogenetic tree building methods. Here, we propose a comparative proteomic and functionomic inferential framework for genome evolution that allows resolving the tripartite division of cells and sketching their history. Evolutionary inferences were derived from the spread of conserved molecular features, such as molecular structures and functions, in the proteomes and functionomes of contemporary organisms. Patterns of use and reuse of these traits yielded significant insights into the origins of cellular diversification. Results uncovered an unprecedented strong evolutionary association between Bacteria and Eukarya while revealing marked evolutionary reductive tendencies in the archaeal genomic repertoires. The effects of nonvertical evolutionary processes (e.g., HGT, convergent evolution) were found to be limited while reductive evolution and molecular innovation appeared to be prevalent during the evolution of cells. Our study revealed a strong vertical trace in the history of proteins and associated molecular functions, which was reliably recovered using the comparative genomics approach. The trace supported the existence of a stem line of descent and the very early appearance of Archaea as a diversified superkingdom, but failed to uncover a hidden canonical pattern in which Bacteria was the first superkingdom to deploy superkingdom-specific structures and functions.
Highlights
Tracing the evolution of extant organisms to a common universal cellular ancestor of life is of fundamental biological importance
Venn diagrams demonstrate the evolutionary sorting of fold superfamily (FSF) and gene ontology (GO) traits in the seven possible and mutually exclusive Venn taxonomic groups, ABE, AB, BE, AE, and the three superkingdom-specific groups, A, B, and E (Figure 2)
Since a Tree of Life” (ToL) by definition is a nested hierarchy of taxonomies, we propose that elevated sharing of traits by a taxonomic group points towards an ancient “vertical trace” indicative of divergence from a common ancestor
Summary
Tracing the evolution of extant organisms to a common universal cellular ancestor of life is of fundamental biological importance. Initial construction of unrooted phylogenies based on the joint evolution of genes linked by an ancient gene duplication event revealed that, for each set of paralogous genes, Archaea and Eukarya were sister groups and diverged from a last archaeal-eukaryal common ancestor [2, 3] This “canonical” rooting that places Bacteria at the base of the “Tree of Life” (ToL) is still widely accepted despite the fact that many other paralogous gene couples produced discordant topologies and despite known technical artifacts associated with these sequence-based evolutionarily deep phylogenies [4, 5]. As a result, reconstructing a truly “universal” ToL portraying the evolutionary relationships of all existing species remains one of the most controversial issues in evolutionary biology This in part owes to the shortcomings of available phylogenetic characters and tree optimization methods that suffer from important technical and conceptual limitations [6, 7] and have failed to generate a consensus.
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