The origin and evolution of viruses inferred from fold family structure

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The origin and evolution of viruses inferred from fold family structure Fizza Mughal1,2 · Arshan Nasir3,4 · Gustavo Caetano‑Anollés1,2  Received: 2 April 2020 / Accepted: 30 May 2020 © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2020

Abstract The canonical frameworks of viral evolution describe viruses as cellular predecessors, reduced forms of cells, or entities that escaped cellular control. The discovery of giant viruses has changed these standard paradigms. Their genetic, proteomic and structural complexities resemble those of cells, prompting a redefinition and reclassification of viruses. In a previous genome-wide analysis of the evolution of structural domains in proteomes, with domains defined at the fold superfamily level, we found the origins of viruses intertwined with those of ancient cells. Here, we extend these data-driven analyses to the study of fold families confirming the co-evolution of viruses and ancient cells and the genetic ability of viruses to foster molecular innovation. The results support our suggestion that viruses arose by genomic reduction from ancient cells and validate a co-evolutionary ‘symbiogenic’ model of viral origins.

Virology in the era of giant viruses The ongoing COVID-19 pandemic [1] is a respiratory illness caused by the rapid global transmission of SARS-CoV-2 [2], the seventh coronavirus known to infect humans. This ravaging disease illustrates the planetary consequences of recurrent episodes of zoonotic transmission from animals to human populations. Pandemics shape public perception. Viruses are seen as noxious agents of infection and death. Pandemics also poise philosophers and virologists to wonder about the origins of viruses and their ability to infect all cellular lineages on Earth [3–7]. Disagreements on whether Handling Editor: Marc H. V. Van Regenmortel. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0070​5-020-04724​-1) contains supplementary material, which is available to authorized users. * Gustavo Caetano‑Anollés [email protected] 1



Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois at UrbanaChampaign, Urbana, IL, USA

2



Illinois Informatics Institute, University of Illinois at Urbana-Champaign, Urbana, IL, USA

3

Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM, USA

4

Department of Biosciences, COMSATS University Islamabad, Islamabad, Pakistan



viruses are living or nonliving persist despite more than a hundred years of virological research and recent data-driven breakthroughs in the field of evolutionary genomics [8–11]. In 2003, the discovery of ‘giant’ viruses [12] revived the debate and challenged epistemological foundations [7, 13]. The size of their genomes rivals that of several parasitic organisms from all three cellular domains (superkingdoms) of life [14]. Their virions, vehicles of transmission that embed the genetic mater