Origins and evolution of viruses of eukaryotes: The ultimate modularity Koonin, E. V., Dolja, V. V., & Krupovic, M. (2015). Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology, 479, 2-25. doi:10.1016/j.virol.2015.02.039 10.1016/j.virol.2015.02.039 Elsevier Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse Virology 479-480 (2015) 2–25 Contents lists available at ScienceDirect Virology journal homepage: www.elsevier.com/locate/yviro Review Origins and evolution of viruses of eukaryotes: The ultimate modularity Eugene V. Koonin a,n, Valerian V. Dolja b, Mart Krupovic c a National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA b Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA c Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Paris 75015, France article info abstract Article history: Viruses and other selfish genetic elements are dominant entities in the biosphere, with respect to both Received 27 January 2015 physical abundance and genetic diversity. Various selfish elements parasitize on all cellular life forms. Returned to author for revisions The relative abundances of different classes of viruses are dramatically different between prokaryotes 19 February 2015 and eukaryotes. In prokaryotes, the great majority of viruses possess double-stranded (ds) DNA Accepted 20 February 2015 genomes, with a substantial minority of single-stranded (ss) DNA viruses and only limited presence of Available online 12 March 2015 RNA viruses. In contrast, in eukaryotes, RNA viruses account for the majority of the virome diversity Keywords: although ssDNA and dsDNA viruses are common as well. Phylogenomic analysis yields tangible clues for Evolution of viruses the origins of major classes of eukaryotic viruses and in particular their likely roots in prokaryotes. Transposable elements Specifically, the ancestral genome of positive-strand RNA viruses of eukaryotes might have been Polintons assembled de novo from genes derived from prokaryotic retroelements and bacteria although a Bacteriophages Recombination primordial origin of this class of viruses cannot be ruled out. Different groups of double-stranded RNA Functional gene modules viruses derive either from dsRNA bacteriophages or from positive-strand RNA viruses. The eukaryotic ssDNA viruses apparently evolved via a fusion of genes from prokaryotic rolling circle-replicating plasmids and positive-strand RNA viruses. Different families of eukaryotic dsDNA viruses appear to have originated from specific groups of bacteriophages on at least two independent occasions. Polintons, the largest known eukaryotic transposons, predicted to also form virus particles, most likely, were the evolutionary intermediates between bacterial tectiviruses and several groups of eukaryotic dsDNA viruses including the proposed order “Megavirales” that unites diverse families of large and giant viruses. Strikingly, evolution of all classes of eukaryotic viruses appears to have involved fusion between structural and replicative gene modules derived from different sources along with additional acquisi- tions of diverse genes. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Contents Introduction..............................................................................................................3 The contrasting viromes of prokaryotes and eukaryotes. 3 Evolutionary scenarios for the origin of eukaryotes and their impact on the reconstruction of virus evolution . 4 Origins of the major classes of eukaryotic viruses and evolutionary relationships between viruses of prokaryotes and eukaryotes . 5 A general perspective on RNA virus evolution: Out of the primordial RNA world?. 5 Positive-strand RNA viruses: Assembly from diverse prokaryotic progenitors and gene exchanges leading to enormous diversification . 6 dsRNA viruses: Multiple origins from positive-strand RNA viruses . 9 Negative-strand RNA viruses: The emerging positive-strand connection. 10 Synopsis on eukaryotic RNA virome. 10 Retroelements and retroviruses: Viruses as derived forms . 10 n Corresponding author. E-mail addresses: [email protected] (E.V. Koonin), [email protected] (V.V. Dolja), [email protected] (M. Krupovic). http://dx.doi.org/10.1016/j.virol.2015.02.039 0042-6822/Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). E.V. Koonin et al. / Virology 479-480 (2015) 2–25 3 Synopsis on eukaryotic retroelements . 14 Origins of ssDNA viruses of eukaryotes: Multiple crosses between plasmids and RNA viruses . 14 Synopsis on ssDNA virus origins. 17 Origins and primary diversification of eukaryotic dsDNA viruses: The bacteriophage and transposable element connections . 17 Synopsis of dsDNA virus evolution. 20 Conclusions.............................................................................................................20 Acknowledgments. 21 Appendix A. Supporting information . 21 References..............................................................................................................21 Introduction viruses and encompass multiple transitions from capsid-less elements A major discovery of environmental genomics over the last to bona fide viruses and vice versa (Koonin and Dolja, 2013, 2014). decade is that the most common and abundant biological entities Thus, any reconstruction of virus evolution that fails to take into on earth are viruses, in particular bacteriophages (Edwards and account the evolutionary relationships with non-viral selfish elements Rohwer, 2005; Rohwer, 2003; Rohwer and Thurber, 2009; Suttle, is bound to be substantially incomplete. The capsid-less elements as 2005, 2007). In marine, soil and animal-associated environments, well as many viruses differ in their extent of integration with the host virus particles consistently outnumber cells by one to two orders of cells: some insert into the cell genome and are transmitted mainly magnitude. Viruses are major ecological and even geological agents vertically through the host generations, others are largely autonomous, that in large part shape such processes as energy conversion in the and many combine both strategies mixed in different proportions. biosphere and sediment formation in water bodies by killing off Viruses and other selfish elements certainly have not evolved populations of abundant, ecologically important organisms such as from a single common ancestor: indeed, not a single gene is cyanobacteria or eukaryotic algae (Fuhrman, 1999; Rohwer and conserved across the entire “greater virus world” or even in the Thurber, 2009; Suttle, 2007). With the possible exception of some majority of selfish elements (Holmes, 2011; Koonin et al., 2006). highly degraded intracellular parasitic bacteria, viruses and/or other However, these elements form a dense evolutionary network in selfish elements, such as transposons and plasmids, parasitize on all which genomes are linked through different shared genes (Koonin cellular organisms. Complementary to their physical dominance in and Dolja, 2014; Krupovic and Koonin, 2015; Yutin et al., 2013). This the biosphere, viruses collectively appear to encompass the bulk of type of evolutionary relationship results from extensive exchange of the genetic diversity on earth (Hendrix, 2003; Kristensen et al., genes and gene modules, in some cases between widely different 2010, 2013). The ubiquity of viruses in the extant biosphere and the elements, as well as parallel capture of homologous genes from the results of theoretical modeling indicating that emergence of selfish hosts by distinct elements. Viruses with large genomes possess genetic elements is intrinsic to any evolving system of replicators numerous genes that were acquired from the hosts at different together imply that virus-host coevolution had been the mode of stages of evolution; such genes typically are restricted in their the evolution of life ever since its origin (Szathmary and Demeter, spread to a narrow group of viruses. However, a small group of viral 1987; Takeuchi and Hogeweg, 2007, 2012; Takeuchi et al., 2011). hallmark genes that encode key proteins involved in genome All cellular life forms possess genomes consisting of double- replication and virion formation and are shared by overlapping sets stranded (ds) DNA and employ the same, standard scheme for repl- of diverse viruses ensures the connectivity of the evolutionary ication and expression. In contrast, viruses and other selfish network in the virus world (Holmes, 2011; Koonin and Dolja, elements exploit all theoretically conceivable inter-conversions of 2014; Koonin et al., 2006). Virus hallmark genes have no obvious nucleic acids, with the genome represented by either RNA or DNA ancestors in cellular life forms, suggesting that virus-like elements that can be either single-stranded or double-stranded, either circ- evolved at a pre-cellular stage of the evolution of life. ular or linear, and consists of either a single or multiple molecules The viromes and mobilomes (i.e. the supersets of viruses and (Agol, 1974; Baltimore, 1971; Koonin, 1991a). Typical viral genomes other selfish elements) of the three domains of cellular life (bacteria, are small compared to genomes of cellular life forms but over the archaea and eukaryotes)