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Title:Structural and functional advances in the evolutionary studies of cells and viruses
Author(s):Nasir, Arshan
Director of Research:Caetano-Anolles, Gustavo
Doctoral Committee Chair(s):Caetano-Anolles, Gustavo
Doctoral Committee Member(s):Mittenthal, Jay; Hudson, Matthew E.; Ma, Jian
Department / Program:Graduate College Programs
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):Gene ontology
Protein structure
Viral evolution
Comparative genomics
Abstract:Phylogenomics aims to describe evolutionary relatedness between organisms by analyzing genomic data. The common practice is to produce phylogenomic trees from molecular information in the sequence, order and content of genes in genomes. These phylogenies describe the evolution of life and have become valuable tools for taxonomy. The recent availability of structural and functional data for hundreds of genomes now offer the opportunity to study evolution using more conserved sets of molecular features. Here we report a phylogenomic (i.e. historical) and comparative (ahistorical) analysis that yields novel insights into the origin of cells (Chapters 1-3) and viruses (Chapters 4-6). We utilized conserved protein domain structure information (fold families [FFs] and fold superfamilies [FSFs]) and ontological definitions of gene products (Gene Ontology [GO]) to reconstruct rooted trees of life (ToL), taking advantage of a genomic census of molecular structure and function in the genomes of sampled organisms and viruses. The analysis revealed a global tendency in the proteomic repertories of cellular organisms to increase domain abundance. ToLs built directly from the census of molecular functions confirmed an early origin of Archaea relative to Bacteria and Eukarya, a conclusion further supported by comparative analysis. The analysis further revealed an ancient history of viruses and their evolution by gene loss. Despite the very high levels of variability seen in the replication strategies, morphologies, and host preferences of extant viruses, we recovered a conserved and ancient structural core of protein domains that was shared between cellular organisms and distantly related viruses. This core together with an analysis of the evolution of virion morphotypes strongly suggests an ancient origin for the viral supergroup. Moreover, a large number of viral proteins lacked cellular homologs and strongly negated the idea that viruses merely evolve by acquiring cellular genes. These virus-specific proteins confer pathogenic abilities to viruses and appeared late in evolution suggesting that the shift to parasitic mode of life happened later in viral evolution. The strong evolutionary association between viruses and cells is likely reminiscent of their ancient co-existence inside primordial cells. Moreover, the crucial dependency of viruses to replicate in an intracellular environment creates fertile grounds for genetic innovation. Interestingly, protein domains shared with viruses were widespread in the proteomes of all three cellular superkingdoms suggesting that viruses mediate gene transfer and crucially enhance biodiversity. The phylogenomic trees identify viruses as a ‘fourth supergroup’ along with cellular superkingdoms, Archaea, Bacteria, and Eukarya. The new model for the origin and evolution of viruses and cells is backed by strong molecular data and is compatible with the existing models of viral evolution. Our experiments indicate that structure and functionomic data represent a useful addition to the set of molecular characters used for tree reconstruction and that ToLs carry in deep branches considerable predictive power to explain the evolution of living organisms and viruses.
Issue Date:2015-01-21
Rights Information:Copyright 2015 Arshan Nasir. Chapters 1, 3, and 5: Creative Commons Attribution License Chapter 2 has been published as manuscript in Journal of Molecular Evolution. See Kim KM, Nasir A, Hwang K, Caetano-Anollés G. (2013) A tree of cellular life inferred from a genomic census of molecular functions. J Mol Evol 79: 240-262. The final publication is available at Authors are allowed to self-archive the author accepted version.
Date Available in IDEALS:2015-07-22
Date Deposited:May 2015

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