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

Abstract

The repertoire of protein architectures in proteomes is evolutionarily conserved and capable of preserving an accurate record of genomic history. Here we use a census of protein architecture in 185 genomes that have been fully sequenced to generate genome-based phylogenies that describe the evolution of the protein world at fold (F) and fold superfamily (FSF) levels. The patterns of representation of F and FSF architectures over evolutionary history suggest three epochs in the evolution of the protein world: (1) architectural diversification, where members of an architecturally rich ancestral community diversified their protein repertoire; (2) superkingdom specification, where superkingdoms Archaea, Bacteria, and Eukarya were specified; and (3) organismal diversification, where F and FSF specific to relatively small sets of organisms appeared as the result of diversification of organismal lineages. Functional annotation of FSF along these architectural chronologies revealed patterns of discovery of biological function. Most importantly, the analysis identified an early and extensive differential loss of architectures occurring primarily in Archaea that segregates the archaeal lineage from the ancient community of organisms and establishes the first organismal divide. Reconstruction of phylogenomic trees of proteomes reflects the timeline of architectural diversification in the emerging lineages. Thus, Archaea undertook a minimalist strategy using only a small subset of the full architectural repertoire and then crystallized into a diversified superkingdom late in evolution. Our analysis also suggests a communal ancestor to all life that was molecularly complex and adopted genomic strategies currently present in Eukarya.

A Dynamic Model for the Evolution of Protein Structure

“…Our results suggest that folds may indeed retain an evolutionary relationship after all. This is not unexpected as a tight correlation between folds and FSFs has been previously noted in several studies [4], [17], and [18]. …”

“…Domination aside, the values of a's increase consistently for both structures until the spike. This spike occurs nearer the end of superkingdom specification and into the epoch of organismal diversification [18]. The analogy we keep in mind is that of a developing field of knowledge.…”

History of biological metal utilization inferred through phylogenomic analysis of protein structures

“…The exact order of closely positioned FSFs is potentially debatable in trees of this size, but trends across the phylogeny are certainly robust and informative (25). For example, Wang et al examined the evolution of protein architectures specific to each superkingdom and delineated the entire phylogeny into three epochs (19). FSFs ubiquitous to life arose during the first epoch (architectural diversification; nd = 0-0.391), and these core architectures catalyze much of modern metabolism, at least in their modern manifestation (19).…”

“…the evolution of the protein world was previously reconstructed by Wang et al (19), and the relative age of each metal-binding architecture was determined from this phylogenomic tree. For visualization, the age of each FSF (node distance, nd) is displayed as the number of nodes from the hypothetical ancestor in the tree on a relative 0 to 1 scale, with nd = 0 representing the birth of the protein universe and nd = 1.0 representing the most recent structural innovation (Fig.…”

“…Here, we expand upon this previous study by examining a larger set of elements and introduce a temporal scale. The relative timing for the evolution of metal-binding protein structures, both those exclusive and promiscuous in metal choice, was determined using a phylogeny of protein architectures that has been developed and refined over the past 7 years (18,19). The occurrences and abundances of all of the diverse Fe-, Zn-, Mn-, Co-, Ni-, Cu-, Mo-, and Ca-binding protein families in 313 genomes were also determined.…”