The spatial arrangements of secondary structures in proteins, irrespective of their connectivity, depict the overall shape and organization of protein domains. These features have been used in the CATH and SCOP classifications to hierarchically partition fold space and define the architectural make up of proteins. Here we use phylogenomic methods and a census of CATH structures in hundreds of genomes to study the origin and diversification of protein architectures (A) and their associated topologies (T) and superfamilies (H). Phylogenies that describe the evolution of domain structures and proteomes were reconstructed from the structural census and used to generate timelines of domain discovery. Phylogenies of CATH domains at T and H levels of structural abstraction and associated chronologies revealed patterns of reductive evolution, the early rise of Archaea, three epochs in the evolution of the protein world, and patterns of structural sharing between Archaea and Eukarya that are very recent. Trees of proteomes confirmed the early appearance of Archaea in the world of organisms. Phylogenies reconstructed from phylogenetic character sets representing T and H domains of different age congruently reflected patterns of domain appearance in the structural chronologies. Trees reconstructed from ancient domain revealed an archaeal rooting. In contrast, trees reconstructed from modern domains exhibited the canonical bacterial rooting. Timelines suggest this rooting is probably driven by patterns of sharing between Archaea and Eukarya. Although CATH and SCOP differ significantly in domain definitions, our findings indicate both classification schemes apportion protein structures on very similar theoretical grounds that harbor similar phylogenetic history. Phylogenies of CATH domains at A level of structural abstraction uncovered general patterns of architectural origin and diversification. The tree of A structures showed that the 3-layer (αβα) sandwich (3.40) and the orthogonal bundle (1.10) that harbor simple secondary structure arrangements are the most ancient, popular and abundant structural designs of proteins. Phylogenies also revealed that ancient A structural designs are comparatively simpler in their makeup and are involved in basic cellular functions. In contrast, modern structural designs such as prisms, propellers, 2-solenoid, super-roll, clam, trefoil and box are not widely distributed and were probably adopted to perform specialized functions. Our timelines therefore uncover a universal tendency towards protein structural complexity that is remarkable.
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